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Journal of Biogeography. 2019;1–15. wileyonlinelibrary.com/journal/jbi | 1 © 2019 John Wiley & Sons Ltd Received: 12 November 2018 | Revised: 31 January 2019 | Accepted: 25 February 2019 DOI: 10.1111/jbi.13563 PERSPECTIVE Pleistocene extinctions as drivers of biogeographical patterns on the easternmost Canary Islands Abstract Subtropical islands are often viewed as refuges where Quaternary climatic shifts driving global episodes of extinction were buffered. Island biodiversity, however, may have been impacted by climatic fluctuations at local scales, particularly in spatially heterogeneous island systems. In this study, we generated a conceptual framework for predicting the potential impact of Pleistocene extinctions on the biogeographical pattern of the Canarian spermatophyte flora, with a focus on the easternmost Canarian islands (ECI). Then, we per - formed an exhaustive bibliographic revision (270 studies) to examine whether taxonomic, phylogenetic and phylogeographical data sup- port our predictions. Although molecular information is limited for many lineages, the available data suggest that the majority of extant ECI plant taxa may be the result of relatively recent (<1 Ma) disper - sal from surrounding insular and mainland areas. Different lines of evidence are compatible with the idea of a Pleistocene period of fre- quent lineage extirpation on ECI. Extinction may thus have provided new ecological opportunities for recent (re)colonization, with some cases of recent establishment mediated by facilitation. Considering background extinction on ECI, we describe five general patterns of colonization for Canarian plant lineages. In addition to factors re- lated to island ontogeny and long-distance dispersal, we suggest that Pleistocene extinctions may have significantly contributed to extant biogeographical patterns in the Canarian archipelago, such as the biased distribution ranges of island plants and the low endemic richness on ECI. This new scenario provides testable hypotheses for future studies dealing with the phylogeography, taxonomy and conservation of terrestrial biodiversity on the Canarian islands, and possibly, on other near-shore islands. 1 | INTRODUCTION Subtropical islands have been long considered as biodiversity refugia (Gibson et al., 2017; Hutsemékers et al., 2011; Sauer, 1969). Unlike most continental areas, climatic stability throughout the Pleistocene is hypothesized to have provided adequate conditions for long- term species persistence in these island systems (Jansson, 2003; Rodriguez-Sanchez & Arroyo, 2008). Extant patterns of biodiver - sity support this view. For instance, Tertiary continental fossils that strongly resemble living insular taxa (Erwin & Schorn, 2000; Kunkel, 1976) pinpoint the role of islands as climatic refugia. In addition, the levels of genetic and species diversity found within insular lineages (Condamine, Leslie, & Antonelli, 2017; García-Verdugo et al., 2013; Kier et al., 2009) suggest that diversification greatly exceeded ex- tinction over geological time. However, recent studies indicate that Pleistocene climatic oscillations may have locally impacted on the biota of subtropical archipelagos (Norder et al., 2019; Prebble et al., 2016; Weigelt, Steinbauer, Sarmento Cabral, & Kreft, 2016). Thus, it is plausible that background extinction on islands could be related to recent climatic events, in addition to abrupt geological episodes (e.g. Marrero & Francisco-Ortega, 2001). If so, both processes may have played a fundamental role in the assembly of certain island biotas, al- though the incidence of extinction in space and time is often difficult to assess (Sanmartín & Meseguer, 2016). The classical island literature depicts the Atlantic archipelagos of Macaronesia (Azores, Madeira, Selvagen, Canary Islands and Cape Verde) as prominent Quaternary refugia of by-gone conti- nental floras (Bramwell, 1976; Cronk, 1997; Kunkel, 1976). Recent molecular approaches are, however, providing new perspectives on the tempo and mode of island colonization. Although previous studies confirm the long-term persistence of several plant lineages (reviewed in Fernández-Palacios et al., 2011; Vargas, 2007), there is mounting evidence that relatively recent (Quaternary) colonizers represent a substantial proportion of the endemic species pool of each archipelago (e.g. Désamoré et al., 2011; Franzke, Sharif Samani, Neuffer, Mummenhoff, & Hurka, 2017; García-Verdugo, Mairal, Monroy, Sajeva, & Caujapé-Castells, 2017; Jones, Reyes-Betancort, Hiscock, & Carine, 2014; Kondraskov et al., 2015). Positive correla- tions between the geological age of a given archipelago and lineage colonization time may be therefore restricted to very few cases (Kondraskov et al., 2015). Rather, molecular reconstructions indicate that multiple waves of island immigrants through time, hybridiza- tion and back-colonization are more common than initially thought (Caujapé-Castells et al., 2017; Emerson, 2002). The high rates of extinction and dispersal underlying such complex patterns are cer - tainly opposed to the static view of islands as temples of relictual- ism or the end of colonization roads (Bellemain & Ricklefs, 2008; Caujapé-Castells, 2004; Patiño et al., 2015). In the context of island colonization, it is remarkable that the po- tential effect of Pleistocene extinction has been rarely addressed in the Atlantic island floras. The few published studies dealing with this process at a regional scale have focused on the interpretation of palaeoenvironmental records (e.g. Genise & Edwards, 2003), and the potential implication of Pliocene episodes of biodiversity loss on Gran Canaria driven by geological events (Anderson, Channing,

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Page 1: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

Journal of Biogeography 20191ndash15 wileyonlinelibrarycomjournaljbi emsp|emsp1copy 2019 John Wiley amp Sons Ltd

Received12November2018emsp |emsp Revised31January2019emsp |emsp Accepted25February2019DOI101111jbi13563

P E R S P E C T I V E

Pleistocene extinctions as drivers of biogeographical patterns on the easternmost Canary Islands

AbstractSubtropical islandsareoftenviewedasrefugeswhereQuaternaryclimaticshiftsdrivingglobalepisodesofextinctionwerebufferedIsland biodiversity howevermay have been impacted by climaticfluctuations at local scales particularly in spatially heterogeneousislandsystemsInthisstudywegeneratedaconceptualframeworkforpredictingthepotentialimpactofPleistoceneextinctionsonthebiogeographicalpatternoftheCanarianspermatophyteflorawitha focus on the easternmost Canarian islands (ECI) Then we per-formedanexhaustivebibliographicrevision(270studies)toexaminewhethertaxonomicphylogeneticandphylogeographicaldatasup-portourpredictionsAlthoughmolecular information is limitedformanylineagestheavailabledatasuggestthatthemajorityofextantECIplanttaxamaybetheresultofrelativelyrecent(lt1Ma)disper-salfromsurrounding insularandmainlandareasDifferent linesofevidencearecompatiblewiththeideaofaPleistoceneperiodoffre-quentlineageextirpationonECIExtinctionmaythushaveprovidednewecologicalopportunitiesforrecent(re)colonizationwithsomecasesofrecentestablishmentmediatedbyfacilitationConsideringbackgroundextinctiononECIwedescribefivegeneralpatternsofcolonization forCanarianplant lineages In addition to factors re-lated to island ontogeny and long-distance dispersal we suggestthat Pleistocene extinctionsmay have significantly contributed toextantbiogeographicalpatternsintheCanarianarchipelagosuchasthebiaseddistributionrangesofislandplantsandthelowendemicrichness on ECI This new scenario provides testable hypothesesforfuturestudiesdealingwiththephylogeographytaxonomyandconservationofterrestrialbiodiversityontheCanarianislandsandpossiblyonothernear-shoreislands

1emsp |emspINTRODUC TION

Subtropicalislandshavebeenlongconsideredasbiodiversityrefugia(Gibsonetal2017Hutsemeacutekersetal2011Sauer1969)UnlikemostcontinentalareasclimaticstabilitythroughoutthePleistoceneis hypothesized to have provided adequate conditions for long-term species persistence in these island systems (Jansson 2003Rodriguez-Sanchez amp Arroyo 2008) Extant patterns of biodiver-sitysupportthisviewForinstanceTertiarycontinentalfossilsthatstronglyresemblelivinginsulartaxa(ErwinampSchorn2000Kunkel1976)pinpointtheroleofislandsasclimaticrefugiaInadditionthelevelsofgeneticandspeciesdiversityfoundwithininsularlineages

(CondamineLeslieampAntonelli2017Garciacutea-Verdugoetal2013Kieretal 2009) suggest thatdiversificationgreatlyexceededex-tinctionovergeologicaltimeHoweverrecentstudiesindicatethatPleistocene climatic oscillationsmayhave locally impactedon thebiotaofsubtropicalarchipelagos(Norderetal2019Prebbleetal2016WeigeltSteinbauerSarmentoCabralampKreft2016)Thusitisplausiblethatbackgroundextinctiononislandscouldberelatedtorecentclimaticeventsinadditiontoabruptgeologicalepisodes(egMarreroampFrancisco-Ortega2001)Ifsobothprocessesmayhaveplayedafundamentalroleintheassemblyofcertainislandbiotasal-thoughtheincidenceofextinctioninspaceandtimeisoftendifficulttoassess(SanmartiacutenampMeseguer2016)

The classical island literature depicts theAtlantic archipelagosof Macaronesia (Azores Madeira Selvagen Canary Islands andCape Verde) as prominent Quaternary refugia of by-gone conti-nental floras (Bramwell 1976Cronk 1997Kunkel 1976)Recentmolecular approaches are however providing new perspectiveson the tempoandmodeof islandcolonizationAlthoughpreviousstudiesconfirmthelong-termpersistenceofseveralplantlineages(reviewed in Fernaacutendez-Palacios etal 2011 Vargas 2007) thereismountingevidencethatrelativelyrecent(Quaternary)colonizersrepresenta substantialproportionof theendemic speciespoolofeacharchipelago(egDeacutesamoreacuteetal2011FranzkeSharifSamaniNeuffer Mummenhoff amp Hurka 2017 Garciacutea-Verdugo MairalMonroySajevaampCaujapeacute-Castells2017JonesReyes-BetancortHiscockampCarine2014Kondraskovetal2015)Positivecorrela-tionsbetweenthegeologicalageofagivenarchipelagoandlineagecolonization time may be therefore restricted to very few cases(Kondraskovetal2015)Rathermolecularreconstructionsindicatethatmultiplewaves of island immigrants through time hybridiza-tionandback-colonizationaremorecommonthaninitiallythought(Caujapeacute-Castells etal 2017 Emerson 2002) The high rates ofextinctionanddispersalunderlyingsuchcomplexpatternsarecer-tainlyopposedtothestaticviewofislandsastemplesofrelictual-ism or the end of colonization roads (BellemainampRicklefs 2008Caujapeacute-Castells2004Patintildeoetal2015)

Inthecontextofislandcolonizationitisremarkablethatthepo-tential effect of Pleistocene extinction has been rarely addressedintheAtlanticislandflorasThefewpublishedstudiesdealingwiththisprocessataregionalscalehavefocusedonthe interpretationofpalaeoenvironmentalrecords(egGeniseampEdwards2003)andthe potential implication of Pliocene episodes of biodiversity lossonGranCanariadrivenbygeologicalevents(AndersonChanning

2emsp |emsp emspensp PERSPECTIVE

amp Zamuner 2009 Emerson 2003 Marrero amp Francisco-Ortega2001)Theimpactofrecentextinctionontheotherhandhasbeenpreferentially linked to human arrival to the islands (ie human-mediatedbiodiversitylossinthelastfewcenturiesdeNascimentoWillis Fernaacutendez-Palacios Criado amp Whittaker 2009 IlleraSpurginRodriguez-ExpositoNogalesampRando2016TerzopoulouRigalWhittakerBorgesampTriantis2015)Tobridge thisgap theaimofthisstudyistoaddressthehypothesisthatPleistoceneep-isodesofbackgroundextinctionmaybelargelyresponsiblefortheextantplantassemblyoftheoldestnear-shoreAtlanticislands(seediscussionsinSanmartiacutenvanderMarkampRonquist2008)

Underequilibriumconditions recent (Quaternary) colonizationofoldislandswouldbeatoddswithclassicalecologicalthinkingonislandbiogeography (reviewed inWhittakerampFernaacutendez-Palacios2007)Predictionsfromthedynamicequilibriummodel(MacArthuramp Wilson 1967) and two hypotheses coined in island systemssuch as the loss of dispersal potential (Carlquist 1974 Cody ampMcOverton1996)andtheniche-preemption(Silvertown2004)an-ticipateaslowpaceofspeciesturnoveronoldvolcanicislandsdue

toecologicallimitationsforsuccessfulimmigrationlossofdispersalpowerwouldreducetheabilityofneighbouringislandresidentstoreachthetarget islandwhereas lowecologicalopportunitywouldhamper the establishment of external diaspores (Carlquist 1974Silvertown2004)

However if an intense period of extinction locally impacts onan archipelago the new non-equilibrium situationwould open upatemporalwindowofrecolonizationduetotheavailabilityofpre-viouslyoccupiednichespace(Carine2005)SuchascenarioholdsespeciallytrueifweconsidertwofactsFirsttheextentofthephe-nomenonoflossofdispersalabilityhasprobablybeengeneralizedwithouttoomuchempiricalsupportEvolutionofdispersalpoten-tialonislandsdoesnotappeartofollowanunidirectionalpatterninplantsandsomelineagesmaybeunaffectedorevenattainhigherpotential for dispersal under insular conditions (Garciacutea-VerdugoCaujapeacute-Castells Mairal ampMonroy 2019 for conceptual discus-sionsseeBurns2018)thusincreasingthelikelihoodofcolonizationfromnearbyislandslessaffectedbyextinctionSecondlargeislandsclose to source areas of potential immigrants are expected to act

F IGURE 1emspComparisonofthespatialconfigurationandemergedsurfaceofthemainCanarianislandsatdifferenttimesthroughouttheQuaternary(alastglacialmaximum20kyrbpbatpresent)extantpatternsofendemicplantspeciesdiversityacrossthetwoeasternmostislands(followingReyes-Betancortetal2008)(c)anddistributionofendemicversusnativenon-endemicplantspeciespoolsacrosstheCanaryIslands(d)

emspensp emsp | emsp3PERSPECTIVE

as strong sinksof colonizers (MacArthurampWilson1967) In sumwepostulatethatunderascenarioofhighextinctionratesspeciesturnover on old islands should be a function of ecological oppor-tunity for rapid colonization a condition thatQuaternary climaticfluctuationsmayhavepromptedonnear-shoreislands

2emsp |emspCONCEPTUAL FR AME WORK

21emsp|emspOverview of the study area

TheCanaryIslandsarepresentlycomposedofsevenmainvolcanicislandswithanE-Wlineararrangementandsubaerialagesrangingfromc20toc1MaHowevertheyonlycorrespondtosixvolcanicedificessincethetwoeasternmostCanarianislands(ECI)LanzaroteandFuerteventurarepresentemergedlandsfromthesamegeologi-calbuildingInadditiontotheirclosegeographicaldistancefromthecontinent(theyarelocatedlt100kmoffthecoastofmainlandNWAfrica)theECIsharesomephysicalattributesthatprovidethemwithsomepeculiaritieswithrespecttothewesternCanaryislands(WCI)ThustheyareamongthefourthlargestislandsinMacaronesiaandshowtheoldestgeologicalage(gt15Mainbothcases)axerophyticclimateandlimitedtopographicalcomplexity(foradetailedphysi-caldescriptionoftheislandsseeJuanEmersonOromiacuteampHewitt2000IlleraDiacuteazampNogales2006)

TheECIalsohaveaparticularontogenyFollowingPleistoceneoscillations the fusion of these two islands and nearby isletsthroughoutrecurrentstadialperiodsresultedinanemergedsurfaceareaknownasMahanthatwasuptotwotimeslargerthanatpres-ent (Figure1a see also Fernaacutendez-Palacios etal 2016) The rela-tivelylowtopologicalcomplexityofMahanprobablyallowedplantandanimaldispersalprovidinggenetichomogeneityacrosstheex-tension of the currently separated islands (Caujapeacute-Castells etal2017) In additionMahanwasmuch closer to neighbouring areas(mainlandAfricaandGranCanaria)thantheislandsofLanzaroteandFuerteventuraaretoday(Figure1ab)AccordingtobiogeographicalpredictionsthephysicalattributesofMahan(ielargeemergedareaandcloseness toother sourcesofpotential colonizers) couldhaveofferedhighopportunities for island colonization (eg Fernaacutendez-Palaciosetal2016)

Thepeculiargeologyof theECI isalso reflected in theirbioticcompositionOnfloristicgroundstheECIareconsideredasadiffer-entsubprovincetothatrepresentedbytheWCI(Reyes-BetancortSantos-GuerraGumaHumphriesampCarine2008)LanzaroteandFuerteventura share a significant proportion of their biodiversitybothintermofspeciesandgeneticvariation(Reyes-Betancortetal2008 Sun Li Vargas-Mendoza Wang amp Xing 2016 ValtuentildeaLoacutepez Alvarez Rodriacuteguez-Riantildeo amp Ortega-Olivencia 2016) andtheirdistinctiveflorahasstrongaffinitieswithmainlandSWMorocco(Meacutedail ampQueacutezel 1999) It is also remarkable that their endemicrichness is largelyconcentratedontheareaswithhighertopologi-calcomplexitymainlyrepresentedbythemassifsofJandiacutea (southFuerteventura) and Famara (north Lanzarote) (Figure1c) EndemicplantrichnessoftheECIhoweverisstrikinglylowwhencompared

tothatoftheWCIbothintermsofsingle-andmultiple-islanden-demics(Acebesetal2010)SuchapatternraisessomequestionsWhyaretheresofewECIendemicsandwhydothefiguresfortheseislandsmatchthoseobservedontheyoungest(c1ndash2Ma)islandsofLaPalmaandElHierroInotherwordswhydoCanarianendemicsmostlyoccuronthewesternislandsPreviousbiogeographicalstud-ieshaveexplainedthisremarkablepatternby invokingtheeffectsofislandontogeny(Caujapeacute-Castellsetal2017WhittakerTriantisampLadle2008)buttoourknowledgenoattemptshavebeenmadetoexaminewhetherrecentepisodesofextinctionfollowedbylim-itedimmigrationmayalsorepresentacontributingfactor(Sanmartiacutenetal2008)

LowhabitatheterogeneityoftenassociatedwiththeadvancederodedstageoftheislandsandsoildegradationhasbeenpostulatedasthemajordriverofthelimitedECIendemicity(Reyes-Betancortetal2008RodriacuteguezRodriacuteguezMoraArbeloampBordon2005)Inadditionhumanimpactisthoughttohavecontributedtogeneratepoorlevelsoftaxonomicdiversityontheseislands(Illeraetal2016Reyes-Betancortetal2008)Unlikeanimaltaxa(GangosoDonaacutezarScholzPalaciosampHiraldo2006Illeraetal2016)human-drivenextinction of Canarian plants has been rarely documented (AedoMedinaBarberaacuteampFernaacutendez-Albert2015Reyes-Betancortetal2008) but may have locally affected extant island distributionsDespitethepotentialimplicationofhumanimpactitishoweverin-terestingtomaketwoobservationswithregardtothelevelsofplantdiversityontheECIFirstthepatternofdistributionofnativenon-endemics (more recent colonizers) in the archipelago clearly doesnotmatchthatofendemics(oldercolonizers)(Figure1d)whichap-pearstosuggestthatcolonizationtimemayalsoplayaroleSecondwhile strong human-mediated pressure (including overgrazing bydomestic ungulates) can affect plant abundance and recruitment(Gangoso etal 2006) it has amore limited impact on thephylo-geographical signal for extant lineages regardlessof their currentabundancerecentphylogeographicalstudiesareprovidingevidencethatsomeECIpopulationsandtaxamayhavehada recentorigineither because theywere the result of dispersal from theWCIorfrommainlandareas(CurtoPuppoKratschmerampMeimberg2017Garciacutea-Verdugoetal2009Stervanderetal2015Valtuentildeaetal2016)A repeatedsignatureacross taxaofsecondarycolonizationoftheECIwithoutevidenceofhybridizationwithputativeoldres-idents is compatible with the idea of broad-scale taxonomic ex-tinction followed by recent immigration Such a possibility albeitfrequentlyhypothesized(CardosoArnedoTriantisampBorges2010Caujapeacute-Castellsetal2017Sanmartiacutenetal2008)hasnotbeenexplicitlyevaluatedtodate

22emsp|emspHypothesis and predictions

OurworkinghypothesisisthatPleistoceneextinctionshadamajorimpact on the biogeographical patterns of the plant species poolof the ECI This hypothesis is framed within the spatio-temporalscenarioprovidedbythese islandsduringthe lastmillionofyearsAlthough the Plio-Pleistocene transition (c26Ma) is formally

4emsp |emsp emspensp PERSPECTIVE

recognizedastheonsetoftheglacialperiodthereisgeneralagree-mentthattheldquomid-Pleistocenetransitionrdquo(MPT)startingataround08Maestablishedanewstageofabruptclimaticshiftswiththestrengthening and lengthening of the glacialndashinterglacial cycles(Loulergueetal2008LoweampWalker2015)Pleistocenecyclesarethoughttohavehadaprofoundimpactonspeciesdistributionsandsurvival rates across islands worldwide (Fernaacutendez-Palacios etal2016Norderetal2019Weigeltetal2016)andislandsclosetocontinentalmassesasclimaticallymarginalareasmighthaveexpe-riencedstronger impacts thanmore isolatedclimaticallymilder is-lands(HardieampHutchings2010)

Climaticpalaeontologicalandphylogeographicalevidenceindi-catethatboththenear-shoreECIandmainlandNWAfricawerepar-ticularly impactedbyclimaticoscillations (Garciacutea-Aloyetal2017Mecoetal2003Ortizetal2006)Sincetheperformanceof is-landsasrefugialargelydependsonthegeographicalextensionandheterogeneityoftheirhabitats(Condamineetal2017GillespieampClague2009)the lowtopographicalcomplexityoftheECIduringthe Quaternary likely offered very few micro-refuges for the

terrestrialbiotawhichconcentratedontheJandiacuteaandFamaramas-sifs (Reyes-Betancort etal 2008)Persistencewasprobablyevenmorechallengingforspecieswithlowervagilitywithspecifichabitatrequirementsorthoserelyingonobligatebioticinteractions(egan-imalpollinationBrodieetal2014)ConverselytheECIcouldhaveactedassinksofimmigrantsthroughoutmesicperiodsduetotheirlarger emerged area close geographical proximity to continentaland island source areas and niche availability following extinction(Figure1a see also Fernaacutendez-Palacios etal 2016) Consideringthese abrupt changes in environmental conditions and ecologicalopportunityovershortevolutionarytimeweanticipatethattheECIflorawouldhavebeensubjecttofrequentextinctionndash(re)coloniza-tioneventsovertheMPT

Inthisstudyweexamineifextantdistributionsofnativeplantsareassociatedwithtemporalpatternsofislandcolonizationdrivenby extinctionWe expect that Quaternary background extinctionmayhave left adetectable signatureonmeasurable traits suchasextantdistributionsandlineagecolonizationtimesThusourpredic-tions(Table1)linkextantdistributionrangestothebiogeographical

TABLE 1emspPredictionslinkingthedistribution(WCI=westernCanarianislandsECI=easternmostCanarianislands)ofextantendemiclineagestimeofislandcolonization(time)andexpectedfrequenciesofplantendemiclineages(lineages)underthehypothesisofPleistoceneextinctionaffectingtheECIColonizationtimeisdividedintotwotemporalwindows(priororafter)withrespecttotheonsetofthemid-Pleistocenetransition(MPTo=08Ma)

Extant distribution Predicted scenarios

WCI ECI Prediction Time LineagesExplanation for the expected of lineages and references

X P1 pre-MPTo HIGH WCIhavehadhighercarryingcapacities(largertotalsizeandhabitatdiversity)thanECIduringthePlio-PleistoceneThereforetheymayhavebufferedMPTfluctuationsmoreefficientlythanECI(1)resultinginoldlineageswithdistributionsaffectedbyECIextirpation(2)

X P2 post-MPTo LOW Becausestepping-stonecolonizationfromECItoWCIisassumedtobethemostplausiblepattern(34)mostrecent(post-MPTo)immigrantsshouldbealsopresentonECI(unlessaffectedbyveryrecentextinction)

X X P3 pre-MPTo HIGH AssumingextinctionthisscenariocouldberepresentedbytwotypesofCanarianendemiclineagesthosewitholdECItaxasurvivingextinctioninsitu(5)andresidentsofneighbouringislandscapableofrecentback-colonizationofECI(6)

X X P4 post-MPTo LOW Stepping-stonecolonizationfromECItoWCIisassumedtobethedominantpattern(34)butextinctionisexpectedtohaveresultedinextensiveislandextirpationofrecentECIimmigrants

X P5 pre-MPTo LOW Old(pre-MPTo)islandlineageswithdistributionsrestrictedtoECIshouldberarebecausethesetwoislandshavefewareasqualifyingasrefuges(7)andendemiclineagestypicallydisplaymulti-islanddistributions(8)

X P6 post-MPTo HIGH Largeislandareashortdispersaldistancesfromsourceareasandhighcarryingcapacity(duetoextinction-drivennicheavailability)enhancelikelihoodofsuccessfulcolonizationofimmigrantsthateventuallydifferentiatefromthesource(910)

Notes(1)Fernaacutendez-Palaciosetal(2016)(2)Caujapeacute-Castellsetal(2017)(3)Juanetal(2000)(4)ShawandGillespie(2016)(5)Juanetal(1998)(6)Curtoetal(2017)(7)Reyes-Betancortetal(2008)(8)Priceetal(2018)(9)MacArthurandWilson(1967)(10)Carine(2005)

emspensp emsp | emsp5PERSPECTIVE

imprintofPleistoceneextinctionsFloristicextirpationsareexpectedto have shaped island lineages regardless ofwhether these colo-nizedthearchipelagobeforeoraftertheintensificationoftheglacialcycles(c08Ma)Basedonpreviousstudies(Juanetal2000ShawampGillespie2016)andthegradientinhabitatcomplexityacrossthearchipelago (Reyes-Betancort etal 2008) we make two assump-tions (a) themost recurrentpatternof islandcolonization initiallyfollowedtheprogressionrule(iedispersalfrommainlandtoECIandsubsequentdispersalfromECItoWCI)(b)theWCIshowedhigherresiliencetoeventualclimaticshiftsthantheECIinthePleistoceneduetolargerhabitatcomplexityandbiggerextensionBycomparingtheavailablesupportforeachsetofpredictions(Table1)weaimattestingthreespatio-temporalscenariosderivedfromthehypothesisofmid-Pleistoceneextinction(a)temporalfilteroflineagedispersaltoWCI(P1+P2predictions)(b)disruptionoftheprogressionrule(P3+P4)and(c)driverofrecentECIimmigrationrates(P5+P6)Tofurthertesttheeffectofcolonizationageondistributionpatternswealsopredictthatnativenon-endemiclineagesunlikeoldislandresident lineagesshoulddisplaydistributionpatternsnotaffectedbyextinctionfilters(iefullycompatiblewiththeprogressionrule)

23emsp|emspLiterature survey

OurstudyfocusedonthespermatophytefloraoftheCanarianarchi-pelagoSomeendemic-richterrestrialgroupshavereceivedconsid-erableattentioninbiogeographicalanalysescentredontheCanaryIslands(Illeraetal2016Juanetal2000Sanmartiacutenetal2008)HoweverinformationforCanarianplantsfarexceedsthatavailablefor animals allowing lineage delimitation for themajority of planttaxaknowntobenativetothearchipelagoRatherthanfocusingonrecognizedtaxonomicspeciesweused island lineagesasobserva-tional units (for similar approaches see Garciacutea-Verdugo BaldwinFayampCaujapeacute-Castells2014Priceetal2018Valenteetal2017)Island lineages were classified as endemic or native non-endemicfollowing the rationale provided in Price etal (2018) Briefly en-demiclineagesweredelimitedusingphylogenetictaxonomicandorpopulation-levelgeneticstudiesthathaveidentifiedgroupsofcloselyrelatedCanarianspeciesorpopulationsstronglydifferentiatedfrommainlandcounterparts(seeAppendixS1inSupportingInformation)Nativenon-endemiclineageswereextractedfromthemostupdatedchecklist of native non-endemic Canarian species (Acebes etal2010)asweconsidereachofthesespeciestorepresentindepend-entcolonizationeventsoftheislandswithoutsubsequentspeciationInthiscaserecordswerelimitedtothoselikelyrepresentingnatu-rallyoccurringlineages(ldquonativosegurordquo=nativewithcertaintyandldquonativoprobablerdquo=likelynative)(Acebesetal2010)

Inadditiontheinformationincludedinthechecklistofthevas-cularplantsfortheCanaryIslands(Acebesetal2010)wasusedasapreliminarysourceforcharacterizationofislanddistributionseventhough itdoesnot implement results fromrecentmolecular stud-iesThenweperformedanexhaustivebibliographicalsearchcon-sideringtaxonomicphylogeneticandphylogeographicalstudiesonCanarianplanttaxaDatafrom254studieswereanalysedtoidentify

thenumberofislandplantlineagesasaccuratelyaspossibleandtoobtaininformationonthebiogeographicalpatternoftheselineages(seeAppendixS1)Distributiondatafromthechecklistofnativelin-eageswereupdatedThussomenativenon-endemiclineagesweretreatedinourstudyasislandendemicswhileotherspeciespopula-tionsformerlyregardedasnativeweretreatedasintroducedwhensupportedbydatapublishedafterAcebesetal(2010)Whenavail-abledivergencetimeestimatesbetweenislandlineagesandcloselyrelatedmainlandtaxawereusedasasurrogateofislandcolonizationThislatterapproachbearshoweversomelimitationsFirstageesti-matesofmoleculardivergencedonotnecessaryreflectcolonizationtimeaccuratelyIncompletetaxonsamplingeitherduetoextinctionof closer relatives or limited representation of continental and is-landspeciesandincompletelineagesortingmayresultinpoorlyre-solvedorincorrectphylogeneticrelationshipswhichleadtobiasedestimatesofcolonizationtimes (seeegEmerson2002EmersonOromiampHewitt2000Stervanderetal2015)Toaccountforthissource of uncertainty we adopted the following approach Firstweestimatedthemostprobablecolonizationtimetobewithintheintervalsetbythestem(divergencefromthecontinentalrelatives)andthecrownage (diversificationwithinthe islandsetting)of theislandlineagewhenbothestimateswereprovidedSecondbecauseestimatesofdivergencetimesdependonthegeneralrateofDNAsubstitutionusedwealsoconsideredtheconfidenceintervalsgen-erated in the studies Lastlywebalanced thequalityof the infor-mationprovidedbyeachstudycaseandthepatterns inferredforlineageswereclassifiedintoldquostrongrdquoorldquomoderaterdquoThusifstudiesprovided divergence time estimates based on phylogenetic rela-tionshipsresolvedwithhigh(iegt90nodalbootstrap)supportfortheECItaxapopulationsthepatternwasclassifiedasldquostrongrdquoBycontrastinferencesweredeemedasldquomoderaterdquoifdivergencewasbasedonlevelsofgeneticdifferentiationandorphylogeneticrecon-structionswithmorelimitedsupport

3emsp |emspSPATIO - TEMPOR AL PAT TERNS

Ourliteraturesurveyallowedidentificationof233plantendemiclin-eages(seeAppendixS1)Wedetectedsomeendemictaxaforwhichassignationtoclearlydefinedislandlineagesisstillhypotheticaldueto the inconclusive information available to date However theseonlyrepresentedasmall fraction(22)ofthetotalOntheotherhandafterexclusionofcasesthatrecentstudieshaveredefinedasendemic or human-introduced native non-endemics were repre-sentedby284lineages

We found significant associations between type of lineage(endemic vs native non-endemic) and extant island distributions(χ2=821plt0001Table2)ThusendemiclineagespreferentiallyoccuronWCI(532ofcases)whereasasmallfractionofthistypeoflineages(c10)isrestrictedtoECI(Table2)Incontrastrecentcolonizers represented by native non-endemic lineages preferen-tially occupy both ECI andWCI (70of the total) and showed asmallnumberofcasesexclusivelyfoundonWCI(158Table2)

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

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Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

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Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

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deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

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PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 2: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

2emsp |emsp emspensp PERSPECTIVE

amp Zamuner 2009 Emerson 2003 Marrero amp Francisco-Ortega2001)Theimpactofrecentextinctionontheotherhandhasbeenpreferentially linked to human arrival to the islands (ie human-mediatedbiodiversitylossinthelastfewcenturiesdeNascimentoWillis Fernaacutendez-Palacios Criado amp Whittaker 2009 IlleraSpurginRodriguez-ExpositoNogalesampRando2016TerzopoulouRigalWhittakerBorgesampTriantis2015)Tobridge thisgap theaimofthisstudyistoaddressthehypothesisthatPleistoceneep-isodesofbackgroundextinctionmaybelargelyresponsiblefortheextantplantassemblyoftheoldestnear-shoreAtlanticislands(seediscussionsinSanmartiacutenvanderMarkampRonquist2008)

Underequilibriumconditions recent (Quaternary) colonizationofoldislandswouldbeatoddswithclassicalecologicalthinkingonislandbiogeography (reviewed inWhittakerampFernaacutendez-Palacios2007)Predictionsfromthedynamicequilibriummodel(MacArthuramp Wilson 1967) and two hypotheses coined in island systemssuch as the loss of dispersal potential (Carlquist 1974 Cody ampMcOverton1996)andtheniche-preemption(Silvertown2004)an-ticipateaslowpaceofspeciesturnoveronoldvolcanicislandsdue

toecologicallimitationsforsuccessfulimmigrationlossofdispersalpowerwouldreducetheabilityofneighbouringislandresidentstoreachthetarget islandwhereas lowecologicalopportunitywouldhamper the establishment of external diaspores (Carlquist 1974Silvertown2004)

However if an intense period of extinction locally impacts onan archipelago the new non-equilibrium situationwould open upatemporalwindowofrecolonizationduetotheavailabilityofpre-viouslyoccupiednichespace(Carine2005)SuchascenarioholdsespeciallytrueifweconsidertwofactsFirsttheextentofthephe-nomenonoflossofdispersalabilityhasprobablybeengeneralizedwithouttoomuchempiricalsupportEvolutionofdispersalpoten-tialonislandsdoesnotappeartofollowanunidirectionalpatterninplantsandsomelineagesmaybeunaffectedorevenattainhigherpotential for dispersal under insular conditions (Garciacutea-VerdugoCaujapeacute-Castells Mairal ampMonroy 2019 for conceptual discus-sionsseeBurns2018)thusincreasingthelikelihoodofcolonizationfromnearbyislandslessaffectedbyextinctionSecondlargeislandsclose to source areas of potential immigrants are expected to act

F IGURE 1emspComparisonofthespatialconfigurationandemergedsurfaceofthemainCanarianislandsatdifferenttimesthroughouttheQuaternary(alastglacialmaximum20kyrbpbatpresent)extantpatternsofendemicplantspeciesdiversityacrossthetwoeasternmostislands(followingReyes-Betancortetal2008)(c)anddistributionofendemicversusnativenon-endemicplantspeciespoolsacrosstheCanaryIslands(d)

emspensp emsp | emsp3PERSPECTIVE

as strong sinksof colonizers (MacArthurampWilson1967) In sumwepostulatethatunderascenarioofhighextinctionratesspeciesturnover on old islands should be a function of ecological oppor-tunity for rapid colonization a condition thatQuaternary climaticfluctuationsmayhavepromptedonnear-shoreislands

2emsp |emspCONCEPTUAL FR AME WORK

21emsp|emspOverview of the study area

TheCanaryIslandsarepresentlycomposedofsevenmainvolcanicislandswithanE-Wlineararrangementandsubaerialagesrangingfromc20toc1MaHowevertheyonlycorrespondtosixvolcanicedificessincethetwoeasternmostCanarianislands(ECI)LanzaroteandFuerteventurarepresentemergedlandsfromthesamegeologi-calbuildingInadditiontotheirclosegeographicaldistancefromthecontinent(theyarelocatedlt100kmoffthecoastofmainlandNWAfrica)theECIsharesomephysicalattributesthatprovidethemwithsomepeculiaritieswithrespecttothewesternCanaryislands(WCI)ThustheyareamongthefourthlargestislandsinMacaronesiaandshowtheoldestgeologicalage(gt15Mainbothcases)axerophyticclimateandlimitedtopographicalcomplexity(foradetailedphysi-caldescriptionoftheislandsseeJuanEmersonOromiacuteampHewitt2000IlleraDiacuteazampNogales2006)

TheECIalsohaveaparticularontogenyFollowingPleistoceneoscillations the fusion of these two islands and nearby isletsthroughoutrecurrentstadialperiodsresultedinanemergedsurfaceareaknownasMahanthatwasuptotwotimeslargerthanatpres-ent (Figure1a see also Fernaacutendez-Palacios etal 2016) The rela-tivelylowtopologicalcomplexityofMahanprobablyallowedplantandanimaldispersalprovidinggenetichomogeneityacrosstheex-tension of the currently separated islands (Caujapeacute-Castells etal2017) In additionMahanwasmuch closer to neighbouring areas(mainlandAfricaandGranCanaria)thantheislandsofLanzaroteandFuerteventuraaretoday(Figure1ab)AccordingtobiogeographicalpredictionsthephysicalattributesofMahan(ielargeemergedareaandcloseness toother sourcesofpotential colonizers) couldhaveofferedhighopportunities for island colonization (eg Fernaacutendez-Palaciosetal2016)

Thepeculiargeologyof theECI isalso reflected in theirbioticcompositionOnfloristicgroundstheECIareconsideredasadiffer-entsubprovincetothatrepresentedbytheWCI(Reyes-BetancortSantos-GuerraGumaHumphriesampCarine2008)LanzaroteandFuerteventura share a significant proportion of their biodiversitybothintermofspeciesandgeneticvariation(Reyes-Betancortetal2008 Sun Li Vargas-Mendoza Wang amp Xing 2016 ValtuentildeaLoacutepez Alvarez Rodriacuteguez-Riantildeo amp Ortega-Olivencia 2016) andtheirdistinctiveflorahasstrongaffinitieswithmainlandSWMorocco(Meacutedail ampQueacutezel 1999) It is also remarkable that their endemicrichness is largelyconcentratedontheareaswithhighertopologi-calcomplexitymainlyrepresentedbythemassifsofJandiacutea (southFuerteventura) and Famara (north Lanzarote) (Figure1c) EndemicplantrichnessoftheECIhoweverisstrikinglylowwhencompared

tothatoftheWCIbothintermsofsingle-andmultiple-islanden-demics(Acebesetal2010)SuchapatternraisessomequestionsWhyaretheresofewECIendemicsandwhydothefiguresfortheseislandsmatchthoseobservedontheyoungest(c1ndash2Ma)islandsofLaPalmaandElHierroInotherwordswhydoCanarianendemicsmostlyoccuronthewesternislandsPreviousbiogeographicalstud-ieshaveexplainedthisremarkablepatternby invokingtheeffectsofislandontogeny(Caujapeacute-Castellsetal2017WhittakerTriantisampLadle2008)buttoourknowledgenoattemptshavebeenmadetoexaminewhetherrecentepisodesofextinctionfollowedbylim-itedimmigrationmayalsorepresentacontributingfactor(Sanmartiacutenetal2008)

LowhabitatheterogeneityoftenassociatedwiththeadvancederodedstageoftheislandsandsoildegradationhasbeenpostulatedasthemajordriverofthelimitedECIendemicity(Reyes-Betancortetal2008RodriacuteguezRodriacuteguezMoraArbeloampBordon2005)Inadditionhumanimpactisthoughttohavecontributedtogeneratepoorlevelsoftaxonomicdiversityontheseislands(Illeraetal2016Reyes-Betancortetal2008)Unlikeanimaltaxa(GangosoDonaacutezarScholzPalaciosampHiraldo2006Illeraetal2016)human-drivenextinction of Canarian plants has been rarely documented (AedoMedinaBarberaacuteampFernaacutendez-Albert2015Reyes-Betancortetal2008) but may have locally affected extant island distributionsDespitethepotentialimplicationofhumanimpactitishoweverin-terestingtomaketwoobservationswithregardtothelevelsofplantdiversityontheECIFirstthepatternofdistributionofnativenon-endemics (more recent colonizers) in the archipelago clearly doesnotmatchthatofendemics(oldercolonizers)(Figure1d)whichap-pearstosuggestthatcolonizationtimemayalsoplayaroleSecondwhile strong human-mediated pressure (including overgrazing bydomestic ungulates) can affect plant abundance and recruitment(Gangoso etal 2006) it has amore limited impact on thephylo-geographical signal for extant lineages regardlessof their currentabundancerecentphylogeographicalstudiesareprovidingevidencethatsomeECIpopulationsandtaxamayhavehada recentorigineither because theywere the result of dispersal from theWCIorfrommainlandareas(CurtoPuppoKratschmerampMeimberg2017Garciacutea-Verdugoetal2009Stervanderetal2015Valtuentildeaetal2016)A repeatedsignatureacross taxaofsecondarycolonizationoftheECIwithoutevidenceofhybridizationwithputativeoldres-idents is compatible with the idea of broad-scale taxonomic ex-tinction followed by recent immigration Such a possibility albeitfrequentlyhypothesized(CardosoArnedoTriantisampBorges2010Caujapeacute-Castellsetal2017Sanmartiacutenetal2008)hasnotbeenexplicitlyevaluatedtodate

22emsp|emspHypothesis and predictions

OurworkinghypothesisisthatPleistoceneextinctionshadamajorimpact on the biogeographical patterns of the plant species poolof the ECI This hypothesis is framed within the spatio-temporalscenarioprovidedbythese islandsduringthe lastmillionofyearsAlthough the Plio-Pleistocene transition (c26Ma) is formally

4emsp |emsp emspensp PERSPECTIVE

recognizedastheonsetoftheglacialperiodthereisgeneralagree-mentthattheldquomid-Pleistocenetransitionrdquo(MPT)startingataround08Maestablishedanewstageofabruptclimaticshiftswiththestrengthening and lengthening of the glacialndashinterglacial cycles(Loulergueetal2008LoweampWalker2015)Pleistocenecyclesarethoughttohavehadaprofoundimpactonspeciesdistributionsandsurvival rates across islands worldwide (Fernaacutendez-Palacios etal2016Norderetal2019Weigeltetal2016)andislandsclosetocontinentalmassesasclimaticallymarginalareasmighthaveexpe-riencedstronger impacts thanmore isolatedclimaticallymilder is-lands(HardieampHutchings2010)

Climaticpalaeontologicalandphylogeographicalevidenceindi-catethatboththenear-shoreECIandmainlandNWAfricawerepar-ticularly impactedbyclimaticoscillations (Garciacutea-Aloyetal2017Mecoetal2003Ortizetal2006)Sincetheperformanceof is-landsasrefugialargelydependsonthegeographicalextensionandheterogeneityoftheirhabitats(Condamineetal2017GillespieampClague2009)the lowtopographicalcomplexityoftheECIduringthe Quaternary likely offered very few micro-refuges for the

terrestrialbiotawhichconcentratedontheJandiacuteaandFamaramas-sifs (Reyes-Betancort etal 2008)Persistencewasprobablyevenmorechallengingforspecieswithlowervagilitywithspecifichabitatrequirementsorthoserelyingonobligatebioticinteractions(egan-imalpollinationBrodieetal2014)ConverselytheECIcouldhaveactedassinksofimmigrantsthroughoutmesicperiodsduetotheirlarger emerged area close geographical proximity to continentaland island source areas and niche availability following extinction(Figure1a see also Fernaacutendez-Palacios etal 2016) Consideringthese abrupt changes in environmental conditions and ecologicalopportunityovershortevolutionarytimeweanticipatethattheECIflorawouldhavebeensubjecttofrequentextinctionndash(re)coloniza-tioneventsovertheMPT

Inthisstudyweexamineifextantdistributionsofnativeplantsareassociatedwithtemporalpatternsofislandcolonizationdrivenby extinctionWe expect that Quaternary background extinctionmayhave left adetectable signatureonmeasurable traits suchasextantdistributionsandlineagecolonizationtimesThusourpredic-tions(Table1)linkextantdistributionrangestothebiogeographical

TABLE 1emspPredictionslinkingthedistribution(WCI=westernCanarianislandsECI=easternmostCanarianislands)ofextantendemiclineagestimeofislandcolonization(time)andexpectedfrequenciesofplantendemiclineages(lineages)underthehypothesisofPleistoceneextinctionaffectingtheECIColonizationtimeisdividedintotwotemporalwindows(priororafter)withrespecttotheonsetofthemid-Pleistocenetransition(MPTo=08Ma)

Extant distribution Predicted scenarios

WCI ECI Prediction Time LineagesExplanation for the expected of lineages and references

X P1 pre-MPTo HIGH WCIhavehadhighercarryingcapacities(largertotalsizeandhabitatdiversity)thanECIduringthePlio-PleistoceneThereforetheymayhavebufferedMPTfluctuationsmoreefficientlythanECI(1)resultinginoldlineageswithdistributionsaffectedbyECIextirpation(2)

X P2 post-MPTo LOW Becausestepping-stonecolonizationfromECItoWCIisassumedtobethemostplausiblepattern(34)mostrecent(post-MPTo)immigrantsshouldbealsopresentonECI(unlessaffectedbyveryrecentextinction)

X X P3 pre-MPTo HIGH AssumingextinctionthisscenariocouldberepresentedbytwotypesofCanarianendemiclineagesthosewitholdECItaxasurvivingextinctioninsitu(5)andresidentsofneighbouringislandscapableofrecentback-colonizationofECI(6)

X X P4 post-MPTo LOW Stepping-stonecolonizationfromECItoWCIisassumedtobethedominantpattern(34)butextinctionisexpectedtohaveresultedinextensiveislandextirpationofrecentECIimmigrants

X P5 pre-MPTo LOW Old(pre-MPTo)islandlineageswithdistributionsrestrictedtoECIshouldberarebecausethesetwoislandshavefewareasqualifyingasrefuges(7)andendemiclineagestypicallydisplaymulti-islanddistributions(8)

X P6 post-MPTo HIGH Largeislandareashortdispersaldistancesfromsourceareasandhighcarryingcapacity(duetoextinction-drivennicheavailability)enhancelikelihoodofsuccessfulcolonizationofimmigrantsthateventuallydifferentiatefromthesource(910)

Notes(1)Fernaacutendez-Palaciosetal(2016)(2)Caujapeacute-Castellsetal(2017)(3)Juanetal(2000)(4)ShawandGillespie(2016)(5)Juanetal(1998)(6)Curtoetal(2017)(7)Reyes-Betancortetal(2008)(8)Priceetal(2018)(9)MacArthurandWilson(1967)(10)Carine(2005)

emspensp emsp | emsp5PERSPECTIVE

imprintofPleistoceneextinctionsFloristicextirpationsareexpectedto have shaped island lineages regardless ofwhether these colo-nizedthearchipelagobeforeoraftertheintensificationoftheglacialcycles(c08Ma)Basedonpreviousstudies(Juanetal2000ShawampGillespie2016)andthegradientinhabitatcomplexityacrossthearchipelago (Reyes-Betancort etal 2008) we make two assump-tions (a) themost recurrentpatternof islandcolonization initiallyfollowedtheprogressionrule(iedispersalfrommainlandtoECIandsubsequentdispersalfromECItoWCI)(b)theWCIshowedhigherresiliencetoeventualclimaticshiftsthantheECIinthePleistoceneduetolargerhabitatcomplexityandbiggerextensionBycomparingtheavailablesupportforeachsetofpredictions(Table1)weaimattestingthreespatio-temporalscenariosderivedfromthehypothesisofmid-Pleistoceneextinction(a)temporalfilteroflineagedispersaltoWCI(P1+P2predictions)(b)disruptionoftheprogressionrule(P3+P4)and(c)driverofrecentECIimmigrationrates(P5+P6)Tofurthertesttheeffectofcolonizationageondistributionpatternswealsopredictthatnativenon-endemiclineagesunlikeoldislandresident lineagesshoulddisplaydistributionpatternsnotaffectedbyextinctionfilters(iefullycompatiblewiththeprogressionrule)

23emsp|emspLiterature survey

OurstudyfocusedonthespermatophytefloraoftheCanarianarchi-pelagoSomeendemic-richterrestrialgroupshavereceivedconsid-erableattentioninbiogeographicalanalysescentredontheCanaryIslands(Illeraetal2016Juanetal2000Sanmartiacutenetal2008)HoweverinformationforCanarianplantsfarexceedsthatavailablefor animals allowing lineage delimitation for themajority of planttaxaknowntobenativetothearchipelagoRatherthanfocusingonrecognizedtaxonomicspeciesweused island lineagesasobserva-tional units (for similar approaches see Garciacutea-Verdugo BaldwinFayampCaujapeacute-Castells2014Priceetal2018Valenteetal2017)Island lineages were classified as endemic or native non-endemicfollowing the rationale provided in Price etal (2018) Briefly en-demiclineagesweredelimitedusingphylogenetictaxonomicandorpopulation-levelgeneticstudiesthathaveidentifiedgroupsofcloselyrelatedCanarianspeciesorpopulationsstronglydifferentiatedfrommainlandcounterparts(seeAppendixS1inSupportingInformation)Nativenon-endemiclineageswereextractedfromthemostupdatedchecklist of native non-endemic Canarian species (Acebes etal2010)asweconsidereachofthesespeciestorepresentindepend-entcolonizationeventsoftheislandswithoutsubsequentspeciationInthiscaserecordswerelimitedtothoselikelyrepresentingnatu-rallyoccurringlineages(ldquonativosegurordquo=nativewithcertaintyandldquonativoprobablerdquo=likelynative)(Acebesetal2010)

Inadditiontheinformationincludedinthechecklistofthevas-cularplantsfortheCanaryIslands(Acebesetal2010)wasusedasapreliminarysourceforcharacterizationofislanddistributionseventhough itdoesnot implement results fromrecentmolecular stud-iesThenweperformedanexhaustivebibliographicalsearchcon-sideringtaxonomicphylogeneticandphylogeographicalstudiesonCanarianplanttaxaDatafrom254studieswereanalysedtoidentify

thenumberofislandplantlineagesasaccuratelyaspossibleandtoobtaininformationonthebiogeographicalpatternoftheselineages(seeAppendixS1)Distributiondatafromthechecklistofnativelin-eageswereupdatedThussomenativenon-endemiclineagesweretreatedinourstudyasislandendemicswhileotherspeciespopula-tionsformerlyregardedasnativeweretreatedasintroducedwhensupportedbydatapublishedafterAcebesetal(2010)Whenavail-abledivergencetimeestimatesbetweenislandlineagesandcloselyrelatedmainlandtaxawereusedasasurrogateofislandcolonizationThislatterapproachbearshoweversomelimitationsFirstageesti-matesofmoleculardivergencedonotnecessaryreflectcolonizationtimeaccuratelyIncompletetaxonsamplingeitherduetoextinctionof closer relatives or limited representation of continental and is-landspeciesandincompletelineagesortingmayresultinpoorlyre-solvedorincorrectphylogeneticrelationshipswhichleadtobiasedestimatesofcolonizationtimes (seeegEmerson2002EmersonOromiampHewitt2000Stervanderetal2015)Toaccountforthissource of uncertainty we adopted the following approach Firstweestimatedthemostprobablecolonizationtimetobewithintheintervalsetbythestem(divergencefromthecontinentalrelatives)andthecrownage (diversificationwithinthe islandsetting)of theislandlineagewhenbothestimateswereprovidedSecondbecauseestimatesofdivergencetimesdependonthegeneralrateofDNAsubstitutionusedwealsoconsideredtheconfidenceintervalsgen-erated in the studies Lastlywebalanced thequalityof the infor-mationprovidedbyeachstudycaseandthepatterns inferredforlineageswereclassifiedintoldquostrongrdquoorldquomoderaterdquoThusifstudiesprovided divergence time estimates based on phylogenetic rela-tionshipsresolvedwithhigh(iegt90nodalbootstrap)supportfortheECItaxapopulationsthepatternwasclassifiedasldquostrongrdquoBycontrastinferencesweredeemedasldquomoderaterdquoifdivergencewasbasedonlevelsofgeneticdifferentiationandorphylogeneticrecon-structionswithmorelimitedsupport

3emsp |emspSPATIO - TEMPOR AL PAT TERNS

Ourliteraturesurveyallowedidentificationof233plantendemiclin-eages(seeAppendixS1)Wedetectedsomeendemictaxaforwhichassignationtoclearlydefinedislandlineagesisstillhypotheticaldueto the inconclusive information available to date However theseonlyrepresentedasmall fraction(22)ofthetotalOntheotherhandafterexclusionofcasesthatrecentstudieshaveredefinedasendemic or human-introduced native non-endemics were repre-sentedby284lineages

We found significant associations between type of lineage(endemic vs native non-endemic) and extant island distributions(χ2=821plt0001Table2)ThusendemiclineagespreferentiallyoccuronWCI(532ofcases)whereasasmallfractionofthistypeoflineages(c10)isrestrictedtoECI(Table2)Incontrastrecentcolonizers represented by native non-endemic lineages preferen-tially occupy both ECI andWCI (70of the total) and showed asmallnumberofcasesexclusivelyfoundonWCI(158Table2)

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

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Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 3: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp3PERSPECTIVE

as strong sinksof colonizers (MacArthurampWilson1967) In sumwepostulatethatunderascenarioofhighextinctionratesspeciesturnover on old islands should be a function of ecological oppor-tunity for rapid colonization a condition thatQuaternary climaticfluctuationsmayhavepromptedonnear-shoreislands

2emsp |emspCONCEPTUAL FR AME WORK

21emsp|emspOverview of the study area

TheCanaryIslandsarepresentlycomposedofsevenmainvolcanicislandswithanE-Wlineararrangementandsubaerialagesrangingfromc20toc1MaHowevertheyonlycorrespondtosixvolcanicedificessincethetwoeasternmostCanarianislands(ECI)LanzaroteandFuerteventurarepresentemergedlandsfromthesamegeologi-calbuildingInadditiontotheirclosegeographicaldistancefromthecontinent(theyarelocatedlt100kmoffthecoastofmainlandNWAfrica)theECIsharesomephysicalattributesthatprovidethemwithsomepeculiaritieswithrespecttothewesternCanaryislands(WCI)ThustheyareamongthefourthlargestislandsinMacaronesiaandshowtheoldestgeologicalage(gt15Mainbothcases)axerophyticclimateandlimitedtopographicalcomplexity(foradetailedphysi-caldescriptionoftheislandsseeJuanEmersonOromiacuteampHewitt2000IlleraDiacuteazampNogales2006)

TheECIalsohaveaparticularontogenyFollowingPleistoceneoscillations the fusion of these two islands and nearby isletsthroughoutrecurrentstadialperiodsresultedinanemergedsurfaceareaknownasMahanthatwasuptotwotimeslargerthanatpres-ent (Figure1a see also Fernaacutendez-Palacios etal 2016) The rela-tivelylowtopologicalcomplexityofMahanprobablyallowedplantandanimaldispersalprovidinggenetichomogeneityacrosstheex-tension of the currently separated islands (Caujapeacute-Castells etal2017) In additionMahanwasmuch closer to neighbouring areas(mainlandAfricaandGranCanaria)thantheislandsofLanzaroteandFuerteventuraaretoday(Figure1ab)AccordingtobiogeographicalpredictionsthephysicalattributesofMahan(ielargeemergedareaandcloseness toother sourcesofpotential colonizers) couldhaveofferedhighopportunities for island colonization (eg Fernaacutendez-Palaciosetal2016)

Thepeculiargeologyof theECI isalso reflected in theirbioticcompositionOnfloristicgroundstheECIareconsideredasadiffer-entsubprovincetothatrepresentedbytheWCI(Reyes-BetancortSantos-GuerraGumaHumphriesampCarine2008)LanzaroteandFuerteventura share a significant proportion of their biodiversitybothintermofspeciesandgeneticvariation(Reyes-Betancortetal2008 Sun Li Vargas-Mendoza Wang amp Xing 2016 ValtuentildeaLoacutepez Alvarez Rodriacuteguez-Riantildeo amp Ortega-Olivencia 2016) andtheirdistinctiveflorahasstrongaffinitieswithmainlandSWMorocco(Meacutedail ampQueacutezel 1999) It is also remarkable that their endemicrichness is largelyconcentratedontheareaswithhighertopologi-calcomplexitymainlyrepresentedbythemassifsofJandiacutea (southFuerteventura) and Famara (north Lanzarote) (Figure1c) EndemicplantrichnessoftheECIhoweverisstrikinglylowwhencompared

tothatoftheWCIbothintermsofsingle-andmultiple-islanden-demics(Acebesetal2010)SuchapatternraisessomequestionsWhyaretheresofewECIendemicsandwhydothefiguresfortheseislandsmatchthoseobservedontheyoungest(c1ndash2Ma)islandsofLaPalmaandElHierroInotherwordswhydoCanarianendemicsmostlyoccuronthewesternislandsPreviousbiogeographicalstud-ieshaveexplainedthisremarkablepatternby invokingtheeffectsofislandontogeny(Caujapeacute-Castellsetal2017WhittakerTriantisampLadle2008)buttoourknowledgenoattemptshavebeenmadetoexaminewhetherrecentepisodesofextinctionfollowedbylim-itedimmigrationmayalsorepresentacontributingfactor(Sanmartiacutenetal2008)

LowhabitatheterogeneityoftenassociatedwiththeadvancederodedstageoftheislandsandsoildegradationhasbeenpostulatedasthemajordriverofthelimitedECIendemicity(Reyes-Betancortetal2008RodriacuteguezRodriacuteguezMoraArbeloampBordon2005)Inadditionhumanimpactisthoughttohavecontributedtogeneratepoorlevelsoftaxonomicdiversityontheseislands(Illeraetal2016Reyes-Betancortetal2008)Unlikeanimaltaxa(GangosoDonaacutezarScholzPalaciosampHiraldo2006Illeraetal2016)human-drivenextinction of Canarian plants has been rarely documented (AedoMedinaBarberaacuteampFernaacutendez-Albert2015Reyes-Betancortetal2008) but may have locally affected extant island distributionsDespitethepotentialimplicationofhumanimpactitishoweverin-terestingtomaketwoobservationswithregardtothelevelsofplantdiversityontheECIFirstthepatternofdistributionofnativenon-endemics (more recent colonizers) in the archipelago clearly doesnotmatchthatofendemics(oldercolonizers)(Figure1d)whichap-pearstosuggestthatcolonizationtimemayalsoplayaroleSecondwhile strong human-mediated pressure (including overgrazing bydomestic ungulates) can affect plant abundance and recruitment(Gangoso etal 2006) it has amore limited impact on thephylo-geographical signal for extant lineages regardlessof their currentabundancerecentphylogeographicalstudiesareprovidingevidencethatsomeECIpopulationsandtaxamayhavehada recentorigineither because theywere the result of dispersal from theWCIorfrommainlandareas(CurtoPuppoKratschmerampMeimberg2017Garciacutea-Verdugoetal2009Stervanderetal2015Valtuentildeaetal2016)A repeatedsignatureacross taxaofsecondarycolonizationoftheECIwithoutevidenceofhybridizationwithputativeoldres-idents is compatible with the idea of broad-scale taxonomic ex-tinction followed by recent immigration Such a possibility albeitfrequentlyhypothesized(CardosoArnedoTriantisampBorges2010Caujapeacute-Castellsetal2017Sanmartiacutenetal2008)hasnotbeenexplicitlyevaluatedtodate

22emsp|emspHypothesis and predictions

OurworkinghypothesisisthatPleistoceneextinctionshadamajorimpact on the biogeographical patterns of the plant species poolof the ECI This hypothesis is framed within the spatio-temporalscenarioprovidedbythese islandsduringthe lastmillionofyearsAlthough the Plio-Pleistocene transition (c26Ma) is formally

4emsp |emsp emspensp PERSPECTIVE

recognizedastheonsetoftheglacialperiodthereisgeneralagree-mentthattheldquomid-Pleistocenetransitionrdquo(MPT)startingataround08Maestablishedanewstageofabruptclimaticshiftswiththestrengthening and lengthening of the glacialndashinterglacial cycles(Loulergueetal2008LoweampWalker2015)Pleistocenecyclesarethoughttohavehadaprofoundimpactonspeciesdistributionsandsurvival rates across islands worldwide (Fernaacutendez-Palacios etal2016Norderetal2019Weigeltetal2016)andislandsclosetocontinentalmassesasclimaticallymarginalareasmighthaveexpe-riencedstronger impacts thanmore isolatedclimaticallymilder is-lands(HardieampHutchings2010)

Climaticpalaeontologicalandphylogeographicalevidenceindi-catethatboththenear-shoreECIandmainlandNWAfricawerepar-ticularly impactedbyclimaticoscillations (Garciacutea-Aloyetal2017Mecoetal2003Ortizetal2006)Sincetheperformanceof is-landsasrefugialargelydependsonthegeographicalextensionandheterogeneityoftheirhabitats(Condamineetal2017GillespieampClague2009)the lowtopographicalcomplexityoftheECIduringthe Quaternary likely offered very few micro-refuges for the

terrestrialbiotawhichconcentratedontheJandiacuteaandFamaramas-sifs (Reyes-Betancort etal 2008)Persistencewasprobablyevenmorechallengingforspecieswithlowervagilitywithspecifichabitatrequirementsorthoserelyingonobligatebioticinteractions(egan-imalpollinationBrodieetal2014)ConverselytheECIcouldhaveactedassinksofimmigrantsthroughoutmesicperiodsduetotheirlarger emerged area close geographical proximity to continentaland island source areas and niche availability following extinction(Figure1a see also Fernaacutendez-Palacios etal 2016) Consideringthese abrupt changes in environmental conditions and ecologicalopportunityovershortevolutionarytimeweanticipatethattheECIflorawouldhavebeensubjecttofrequentextinctionndash(re)coloniza-tioneventsovertheMPT

Inthisstudyweexamineifextantdistributionsofnativeplantsareassociatedwithtemporalpatternsofislandcolonizationdrivenby extinctionWe expect that Quaternary background extinctionmayhave left adetectable signatureonmeasurable traits suchasextantdistributionsandlineagecolonizationtimesThusourpredic-tions(Table1)linkextantdistributionrangestothebiogeographical

TABLE 1emspPredictionslinkingthedistribution(WCI=westernCanarianislandsECI=easternmostCanarianislands)ofextantendemiclineagestimeofislandcolonization(time)andexpectedfrequenciesofplantendemiclineages(lineages)underthehypothesisofPleistoceneextinctionaffectingtheECIColonizationtimeisdividedintotwotemporalwindows(priororafter)withrespecttotheonsetofthemid-Pleistocenetransition(MPTo=08Ma)

Extant distribution Predicted scenarios

WCI ECI Prediction Time LineagesExplanation for the expected of lineages and references

X P1 pre-MPTo HIGH WCIhavehadhighercarryingcapacities(largertotalsizeandhabitatdiversity)thanECIduringthePlio-PleistoceneThereforetheymayhavebufferedMPTfluctuationsmoreefficientlythanECI(1)resultinginoldlineageswithdistributionsaffectedbyECIextirpation(2)

X P2 post-MPTo LOW Becausestepping-stonecolonizationfromECItoWCIisassumedtobethemostplausiblepattern(34)mostrecent(post-MPTo)immigrantsshouldbealsopresentonECI(unlessaffectedbyveryrecentextinction)

X X P3 pre-MPTo HIGH AssumingextinctionthisscenariocouldberepresentedbytwotypesofCanarianendemiclineagesthosewitholdECItaxasurvivingextinctioninsitu(5)andresidentsofneighbouringislandscapableofrecentback-colonizationofECI(6)

X X P4 post-MPTo LOW Stepping-stonecolonizationfromECItoWCIisassumedtobethedominantpattern(34)butextinctionisexpectedtohaveresultedinextensiveislandextirpationofrecentECIimmigrants

X P5 pre-MPTo LOW Old(pre-MPTo)islandlineageswithdistributionsrestrictedtoECIshouldberarebecausethesetwoislandshavefewareasqualifyingasrefuges(7)andendemiclineagestypicallydisplaymulti-islanddistributions(8)

X P6 post-MPTo HIGH Largeislandareashortdispersaldistancesfromsourceareasandhighcarryingcapacity(duetoextinction-drivennicheavailability)enhancelikelihoodofsuccessfulcolonizationofimmigrantsthateventuallydifferentiatefromthesource(910)

Notes(1)Fernaacutendez-Palaciosetal(2016)(2)Caujapeacute-Castellsetal(2017)(3)Juanetal(2000)(4)ShawandGillespie(2016)(5)Juanetal(1998)(6)Curtoetal(2017)(7)Reyes-Betancortetal(2008)(8)Priceetal(2018)(9)MacArthurandWilson(1967)(10)Carine(2005)

emspensp emsp | emsp5PERSPECTIVE

imprintofPleistoceneextinctionsFloristicextirpationsareexpectedto have shaped island lineages regardless ofwhether these colo-nizedthearchipelagobeforeoraftertheintensificationoftheglacialcycles(c08Ma)Basedonpreviousstudies(Juanetal2000ShawampGillespie2016)andthegradientinhabitatcomplexityacrossthearchipelago (Reyes-Betancort etal 2008) we make two assump-tions (a) themost recurrentpatternof islandcolonization initiallyfollowedtheprogressionrule(iedispersalfrommainlandtoECIandsubsequentdispersalfromECItoWCI)(b)theWCIshowedhigherresiliencetoeventualclimaticshiftsthantheECIinthePleistoceneduetolargerhabitatcomplexityandbiggerextensionBycomparingtheavailablesupportforeachsetofpredictions(Table1)weaimattestingthreespatio-temporalscenariosderivedfromthehypothesisofmid-Pleistoceneextinction(a)temporalfilteroflineagedispersaltoWCI(P1+P2predictions)(b)disruptionoftheprogressionrule(P3+P4)and(c)driverofrecentECIimmigrationrates(P5+P6)Tofurthertesttheeffectofcolonizationageondistributionpatternswealsopredictthatnativenon-endemiclineagesunlikeoldislandresident lineagesshoulddisplaydistributionpatternsnotaffectedbyextinctionfilters(iefullycompatiblewiththeprogressionrule)

23emsp|emspLiterature survey

OurstudyfocusedonthespermatophytefloraoftheCanarianarchi-pelagoSomeendemic-richterrestrialgroupshavereceivedconsid-erableattentioninbiogeographicalanalysescentredontheCanaryIslands(Illeraetal2016Juanetal2000Sanmartiacutenetal2008)HoweverinformationforCanarianplantsfarexceedsthatavailablefor animals allowing lineage delimitation for themajority of planttaxaknowntobenativetothearchipelagoRatherthanfocusingonrecognizedtaxonomicspeciesweused island lineagesasobserva-tional units (for similar approaches see Garciacutea-Verdugo BaldwinFayampCaujapeacute-Castells2014Priceetal2018Valenteetal2017)Island lineages were classified as endemic or native non-endemicfollowing the rationale provided in Price etal (2018) Briefly en-demiclineagesweredelimitedusingphylogenetictaxonomicandorpopulation-levelgeneticstudiesthathaveidentifiedgroupsofcloselyrelatedCanarianspeciesorpopulationsstronglydifferentiatedfrommainlandcounterparts(seeAppendixS1inSupportingInformation)Nativenon-endemiclineageswereextractedfromthemostupdatedchecklist of native non-endemic Canarian species (Acebes etal2010)asweconsidereachofthesespeciestorepresentindepend-entcolonizationeventsoftheislandswithoutsubsequentspeciationInthiscaserecordswerelimitedtothoselikelyrepresentingnatu-rallyoccurringlineages(ldquonativosegurordquo=nativewithcertaintyandldquonativoprobablerdquo=likelynative)(Acebesetal2010)

Inadditiontheinformationincludedinthechecklistofthevas-cularplantsfortheCanaryIslands(Acebesetal2010)wasusedasapreliminarysourceforcharacterizationofislanddistributionseventhough itdoesnot implement results fromrecentmolecular stud-iesThenweperformedanexhaustivebibliographicalsearchcon-sideringtaxonomicphylogeneticandphylogeographicalstudiesonCanarianplanttaxaDatafrom254studieswereanalysedtoidentify

thenumberofislandplantlineagesasaccuratelyaspossibleandtoobtaininformationonthebiogeographicalpatternoftheselineages(seeAppendixS1)Distributiondatafromthechecklistofnativelin-eageswereupdatedThussomenativenon-endemiclineagesweretreatedinourstudyasislandendemicswhileotherspeciespopula-tionsformerlyregardedasnativeweretreatedasintroducedwhensupportedbydatapublishedafterAcebesetal(2010)Whenavail-abledivergencetimeestimatesbetweenislandlineagesandcloselyrelatedmainlandtaxawereusedasasurrogateofislandcolonizationThislatterapproachbearshoweversomelimitationsFirstageesti-matesofmoleculardivergencedonotnecessaryreflectcolonizationtimeaccuratelyIncompletetaxonsamplingeitherduetoextinctionof closer relatives or limited representation of continental and is-landspeciesandincompletelineagesortingmayresultinpoorlyre-solvedorincorrectphylogeneticrelationshipswhichleadtobiasedestimatesofcolonizationtimes (seeegEmerson2002EmersonOromiampHewitt2000Stervanderetal2015)Toaccountforthissource of uncertainty we adopted the following approach Firstweestimatedthemostprobablecolonizationtimetobewithintheintervalsetbythestem(divergencefromthecontinentalrelatives)andthecrownage (diversificationwithinthe islandsetting)of theislandlineagewhenbothestimateswereprovidedSecondbecauseestimatesofdivergencetimesdependonthegeneralrateofDNAsubstitutionusedwealsoconsideredtheconfidenceintervalsgen-erated in the studies Lastlywebalanced thequalityof the infor-mationprovidedbyeachstudycaseandthepatterns inferredforlineageswereclassifiedintoldquostrongrdquoorldquomoderaterdquoThusifstudiesprovided divergence time estimates based on phylogenetic rela-tionshipsresolvedwithhigh(iegt90nodalbootstrap)supportfortheECItaxapopulationsthepatternwasclassifiedasldquostrongrdquoBycontrastinferencesweredeemedasldquomoderaterdquoifdivergencewasbasedonlevelsofgeneticdifferentiationandorphylogeneticrecon-structionswithmorelimitedsupport

3emsp |emspSPATIO - TEMPOR AL PAT TERNS

Ourliteraturesurveyallowedidentificationof233plantendemiclin-eages(seeAppendixS1)Wedetectedsomeendemictaxaforwhichassignationtoclearlydefinedislandlineagesisstillhypotheticaldueto the inconclusive information available to date However theseonlyrepresentedasmall fraction(22)ofthetotalOntheotherhandafterexclusionofcasesthatrecentstudieshaveredefinedasendemic or human-introduced native non-endemics were repre-sentedby284lineages

We found significant associations between type of lineage(endemic vs native non-endemic) and extant island distributions(χ2=821plt0001Table2)ThusendemiclineagespreferentiallyoccuronWCI(532ofcases)whereasasmallfractionofthistypeoflineages(c10)isrestrictedtoECI(Table2)Incontrastrecentcolonizers represented by native non-endemic lineages preferen-tially occupy both ECI andWCI (70of the total) and showed asmallnumberofcasesexclusivelyfoundonWCI(158Table2)

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 4: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

4emsp |emsp emspensp PERSPECTIVE

recognizedastheonsetoftheglacialperiodthereisgeneralagree-mentthattheldquomid-Pleistocenetransitionrdquo(MPT)startingataround08Maestablishedanewstageofabruptclimaticshiftswiththestrengthening and lengthening of the glacialndashinterglacial cycles(Loulergueetal2008LoweampWalker2015)Pleistocenecyclesarethoughttohavehadaprofoundimpactonspeciesdistributionsandsurvival rates across islands worldwide (Fernaacutendez-Palacios etal2016Norderetal2019Weigeltetal2016)andislandsclosetocontinentalmassesasclimaticallymarginalareasmighthaveexpe-riencedstronger impacts thanmore isolatedclimaticallymilder is-lands(HardieampHutchings2010)

Climaticpalaeontologicalandphylogeographicalevidenceindi-catethatboththenear-shoreECIandmainlandNWAfricawerepar-ticularly impactedbyclimaticoscillations (Garciacutea-Aloyetal2017Mecoetal2003Ortizetal2006)Sincetheperformanceof is-landsasrefugialargelydependsonthegeographicalextensionandheterogeneityoftheirhabitats(Condamineetal2017GillespieampClague2009)the lowtopographicalcomplexityoftheECIduringthe Quaternary likely offered very few micro-refuges for the

terrestrialbiotawhichconcentratedontheJandiacuteaandFamaramas-sifs (Reyes-Betancort etal 2008)Persistencewasprobablyevenmorechallengingforspecieswithlowervagilitywithspecifichabitatrequirementsorthoserelyingonobligatebioticinteractions(egan-imalpollinationBrodieetal2014)ConverselytheECIcouldhaveactedassinksofimmigrantsthroughoutmesicperiodsduetotheirlarger emerged area close geographical proximity to continentaland island source areas and niche availability following extinction(Figure1a see also Fernaacutendez-Palacios etal 2016) Consideringthese abrupt changes in environmental conditions and ecologicalopportunityovershortevolutionarytimeweanticipatethattheECIflorawouldhavebeensubjecttofrequentextinctionndash(re)coloniza-tioneventsovertheMPT

Inthisstudyweexamineifextantdistributionsofnativeplantsareassociatedwithtemporalpatternsofislandcolonizationdrivenby extinctionWe expect that Quaternary background extinctionmayhave left adetectable signatureonmeasurable traits suchasextantdistributionsandlineagecolonizationtimesThusourpredic-tions(Table1)linkextantdistributionrangestothebiogeographical

TABLE 1emspPredictionslinkingthedistribution(WCI=westernCanarianislandsECI=easternmostCanarianislands)ofextantendemiclineagestimeofislandcolonization(time)andexpectedfrequenciesofplantendemiclineages(lineages)underthehypothesisofPleistoceneextinctionaffectingtheECIColonizationtimeisdividedintotwotemporalwindows(priororafter)withrespecttotheonsetofthemid-Pleistocenetransition(MPTo=08Ma)

Extant distribution Predicted scenarios

WCI ECI Prediction Time LineagesExplanation for the expected of lineages and references

X P1 pre-MPTo HIGH WCIhavehadhighercarryingcapacities(largertotalsizeandhabitatdiversity)thanECIduringthePlio-PleistoceneThereforetheymayhavebufferedMPTfluctuationsmoreefficientlythanECI(1)resultinginoldlineageswithdistributionsaffectedbyECIextirpation(2)

X P2 post-MPTo LOW Becausestepping-stonecolonizationfromECItoWCIisassumedtobethemostplausiblepattern(34)mostrecent(post-MPTo)immigrantsshouldbealsopresentonECI(unlessaffectedbyveryrecentextinction)

X X P3 pre-MPTo HIGH AssumingextinctionthisscenariocouldberepresentedbytwotypesofCanarianendemiclineagesthosewitholdECItaxasurvivingextinctioninsitu(5)andresidentsofneighbouringislandscapableofrecentback-colonizationofECI(6)

X X P4 post-MPTo LOW Stepping-stonecolonizationfromECItoWCIisassumedtobethedominantpattern(34)butextinctionisexpectedtohaveresultedinextensiveislandextirpationofrecentECIimmigrants

X P5 pre-MPTo LOW Old(pre-MPTo)islandlineageswithdistributionsrestrictedtoECIshouldberarebecausethesetwoislandshavefewareasqualifyingasrefuges(7)andendemiclineagestypicallydisplaymulti-islanddistributions(8)

X P6 post-MPTo HIGH Largeislandareashortdispersaldistancesfromsourceareasandhighcarryingcapacity(duetoextinction-drivennicheavailability)enhancelikelihoodofsuccessfulcolonizationofimmigrantsthateventuallydifferentiatefromthesource(910)

Notes(1)Fernaacutendez-Palaciosetal(2016)(2)Caujapeacute-Castellsetal(2017)(3)Juanetal(2000)(4)ShawandGillespie(2016)(5)Juanetal(1998)(6)Curtoetal(2017)(7)Reyes-Betancortetal(2008)(8)Priceetal(2018)(9)MacArthurandWilson(1967)(10)Carine(2005)

emspensp emsp | emsp5PERSPECTIVE

imprintofPleistoceneextinctionsFloristicextirpationsareexpectedto have shaped island lineages regardless ofwhether these colo-nizedthearchipelagobeforeoraftertheintensificationoftheglacialcycles(c08Ma)Basedonpreviousstudies(Juanetal2000ShawampGillespie2016)andthegradientinhabitatcomplexityacrossthearchipelago (Reyes-Betancort etal 2008) we make two assump-tions (a) themost recurrentpatternof islandcolonization initiallyfollowedtheprogressionrule(iedispersalfrommainlandtoECIandsubsequentdispersalfromECItoWCI)(b)theWCIshowedhigherresiliencetoeventualclimaticshiftsthantheECIinthePleistoceneduetolargerhabitatcomplexityandbiggerextensionBycomparingtheavailablesupportforeachsetofpredictions(Table1)weaimattestingthreespatio-temporalscenariosderivedfromthehypothesisofmid-Pleistoceneextinction(a)temporalfilteroflineagedispersaltoWCI(P1+P2predictions)(b)disruptionoftheprogressionrule(P3+P4)and(c)driverofrecentECIimmigrationrates(P5+P6)Tofurthertesttheeffectofcolonizationageondistributionpatternswealsopredictthatnativenon-endemiclineagesunlikeoldislandresident lineagesshoulddisplaydistributionpatternsnotaffectedbyextinctionfilters(iefullycompatiblewiththeprogressionrule)

23emsp|emspLiterature survey

OurstudyfocusedonthespermatophytefloraoftheCanarianarchi-pelagoSomeendemic-richterrestrialgroupshavereceivedconsid-erableattentioninbiogeographicalanalysescentredontheCanaryIslands(Illeraetal2016Juanetal2000Sanmartiacutenetal2008)HoweverinformationforCanarianplantsfarexceedsthatavailablefor animals allowing lineage delimitation for themajority of planttaxaknowntobenativetothearchipelagoRatherthanfocusingonrecognizedtaxonomicspeciesweused island lineagesasobserva-tional units (for similar approaches see Garciacutea-Verdugo BaldwinFayampCaujapeacute-Castells2014Priceetal2018Valenteetal2017)Island lineages were classified as endemic or native non-endemicfollowing the rationale provided in Price etal (2018) Briefly en-demiclineagesweredelimitedusingphylogenetictaxonomicandorpopulation-levelgeneticstudiesthathaveidentifiedgroupsofcloselyrelatedCanarianspeciesorpopulationsstronglydifferentiatedfrommainlandcounterparts(seeAppendixS1inSupportingInformation)Nativenon-endemiclineageswereextractedfromthemostupdatedchecklist of native non-endemic Canarian species (Acebes etal2010)asweconsidereachofthesespeciestorepresentindepend-entcolonizationeventsoftheislandswithoutsubsequentspeciationInthiscaserecordswerelimitedtothoselikelyrepresentingnatu-rallyoccurringlineages(ldquonativosegurordquo=nativewithcertaintyandldquonativoprobablerdquo=likelynative)(Acebesetal2010)

Inadditiontheinformationincludedinthechecklistofthevas-cularplantsfortheCanaryIslands(Acebesetal2010)wasusedasapreliminarysourceforcharacterizationofislanddistributionseventhough itdoesnot implement results fromrecentmolecular stud-iesThenweperformedanexhaustivebibliographicalsearchcon-sideringtaxonomicphylogeneticandphylogeographicalstudiesonCanarianplanttaxaDatafrom254studieswereanalysedtoidentify

thenumberofislandplantlineagesasaccuratelyaspossibleandtoobtaininformationonthebiogeographicalpatternoftheselineages(seeAppendixS1)Distributiondatafromthechecklistofnativelin-eageswereupdatedThussomenativenon-endemiclineagesweretreatedinourstudyasislandendemicswhileotherspeciespopula-tionsformerlyregardedasnativeweretreatedasintroducedwhensupportedbydatapublishedafterAcebesetal(2010)Whenavail-abledivergencetimeestimatesbetweenislandlineagesandcloselyrelatedmainlandtaxawereusedasasurrogateofislandcolonizationThislatterapproachbearshoweversomelimitationsFirstageesti-matesofmoleculardivergencedonotnecessaryreflectcolonizationtimeaccuratelyIncompletetaxonsamplingeitherduetoextinctionof closer relatives or limited representation of continental and is-landspeciesandincompletelineagesortingmayresultinpoorlyre-solvedorincorrectphylogeneticrelationshipswhichleadtobiasedestimatesofcolonizationtimes (seeegEmerson2002EmersonOromiampHewitt2000Stervanderetal2015)Toaccountforthissource of uncertainty we adopted the following approach Firstweestimatedthemostprobablecolonizationtimetobewithintheintervalsetbythestem(divergencefromthecontinentalrelatives)andthecrownage (diversificationwithinthe islandsetting)of theislandlineagewhenbothestimateswereprovidedSecondbecauseestimatesofdivergencetimesdependonthegeneralrateofDNAsubstitutionusedwealsoconsideredtheconfidenceintervalsgen-erated in the studies Lastlywebalanced thequalityof the infor-mationprovidedbyeachstudycaseandthepatterns inferredforlineageswereclassifiedintoldquostrongrdquoorldquomoderaterdquoThusifstudiesprovided divergence time estimates based on phylogenetic rela-tionshipsresolvedwithhigh(iegt90nodalbootstrap)supportfortheECItaxapopulationsthepatternwasclassifiedasldquostrongrdquoBycontrastinferencesweredeemedasldquomoderaterdquoifdivergencewasbasedonlevelsofgeneticdifferentiationandorphylogeneticrecon-structionswithmorelimitedsupport

3emsp |emspSPATIO - TEMPOR AL PAT TERNS

Ourliteraturesurveyallowedidentificationof233plantendemiclin-eages(seeAppendixS1)Wedetectedsomeendemictaxaforwhichassignationtoclearlydefinedislandlineagesisstillhypotheticaldueto the inconclusive information available to date However theseonlyrepresentedasmall fraction(22)ofthetotalOntheotherhandafterexclusionofcasesthatrecentstudieshaveredefinedasendemic or human-introduced native non-endemics were repre-sentedby284lineages

We found significant associations between type of lineage(endemic vs native non-endemic) and extant island distributions(χ2=821plt0001Table2)ThusendemiclineagespreferentiallyoccuronWCI(532ofcases)whereasasmallfractionofthistypeoflineages(c10)isrestrictedtoECI(Table2)Incontrastrecentcolonizers represented by native non-endemic lineages preferen-tially occupy both ECI andWCI (70of the total) and showed asmallnumberofcasesexclusivelyfoundonWCI(158Table2)

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

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AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

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WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 5: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp5PERSPECTIVE

imprintofPleistoceneextinctionsFloristicextirpationsareexpectedto have shaped island lineages regardless ofwhether these colo-nizedthearchipelagobeforeoraftertheintensificationoftheglacialcycles(c08Ma)Basedonpreviousstudies(Juanetal2000ShawampGillespie2016)andthegradientinhabitatcomplexityacrossthearchipelago (Reyes-Betancort etal 2008) we make two assump-tions (a) themost recurrentpatternof islandcolonization initiallyfollowedtheprogressionrule(iedispersalfrommainlandtoECIandsubsequentdispersalfromECItoWCI)(b)theWCIshowedhigherresiliencetoeventualclimaticshiftsthantheECIinthePleistoceneduetolargerhabitatcomplexityandbiggerextensionBycomparingtheavailablesupportforeachsetofpredictions(Table1)weaimattestingthreespatio-temporalscenariosderivedfromthehypothesisofmid-Pleistoceneextinction(a)temporalfilteroflineagedispersaltoWCI(P1+P2predictions)(b)disruptionoftheprogressionrule(P3+P4)and(c)driverofrecentECIimmigrationrates(P5+P6)Tofurthertesttheeffectofcolonizationageondistributionpatternswealsopredictthatnativenon-endemiclineagesunlikeoldislandresident lineagesshoulddisplaydistributionpatternsnotaffectedbyextinctionfilters(iefullycompatiblewiththeprogressionrule)

23emsp|emspLiterature survey

OurstudyfocusedonthespermatophytefloraoftheCanarianarchi-pelagoSomeendemic-richterrestrialgroupshavereceivedconsid-erableattentioninbiogeographicalanalysescentredontheCanaryIslands(Illeraetal2016Juanetal2000Sanmartiacutenetal2008)HoweverinformationforCanarianplantsfarexceedsthatavailablefor animals allowing lineage delimitation for themajority of planttaxaknowntobenativetothearchipelagoRatherthanfocusingonrecognizedtaxonomicspeciesweused island lineagesasobserva-tional units (for similar approaches see Garciacutea-Verdugo BaldwinFayampCaujapeacute-Castells2014Priceetal2018Valenteetal2017)Island lineages were classified as endemic or native non-endemicfollowing the rationale provided in Price etal (2018) Briefly en-demiclineagesweredelimitedusingphylogenetictaxonomicandorpopulation-levelgeneticstudiesthathaveidentifiedgroupsofcloselyrelatedCanarianspeciesorpopulationsstronglydifferentiatedfrommainlandcounterparts(seeAppendixS1inSupportingInformation)Nativenon-endemiclineageswereextractedfromthemostupdatedchecklist of native non-endemic Canarian species (Acebes etal2010)asweconsidereachofthesespeciestorepresentindepend-entcolonizationeventsoftheislandswithoutsubsequentspeciationInthiscaserecordswerelimitedtothoselikelyrepresentingnatu-rallyoccurringlineages(ldquonativosegurordquo=nativewithcertaintyandldquonativoprobablerdquo=likelynative)(Acebesetal2010)

Inadditiontheinformationincludedinthechecklistofthevas-cularplantsfortheCanaryIslands(Acebesetal2010)wasusedasapreliminarysourceforcharacterizationofislanddistributionseventhough itdoesnot implement results fromrecentmolecular stud-iesThenweperformedanexhaustivebibliographicalsearchcon-sideringtaxonomicphylogeneticandphylogeographicalstudiesonCanarianplanttaxaDatafrom254studieswereanalysedtoidentify

thenumberofislandplantlineagesasaccuratelyaspossibleandtoobtaininformationonthebiogeographicalpatternoftheselineages(seeAppendixS1)Distributiondatafromthechecklistofnativelin-eageswereupdatedThussomenativenon-endemiclineagesweretreatedinourstudyasislandendemicswhileotherspeciespopula-tionsformerlyregardedasnativeweretreatedasintroducedwhensupportedbydatapublishedafterAcebesetal(2010)Whenavail-abledivergencetimeestimatesbetweenislandlineagesandcloselyrelatedmainlandtaxawereusedasasurrogateofislandcolonizationThislatterapproachbearshoweversomelimitationsFirstageesti-matesofmoleculardivergencedonotnecessaryreflectcolonizationtimeaccuratelyIncompletetaxonsamplingeitherduetoextinctionof closer relatives or limited representation of continental and is-landspeciesandincompletelineagesortingmayresultinpoorlyre-solvedorincorrectphylogeneticrelationshipswhichleadtobiasedestimatesofcolonizationtimes (seeegEmerson2002EmersonOromiampHewitt2000Stervanderetal2015)Toaccountforthissource of uncertainty we adopted the following approach Firstweestimatedthemostprobablecolonizationtimetobewithintheintervalsetbythestem(divergencefromthecontinentalrelatives)andthecrownage (diversificationwithinthe islandsetting)of theislandlineagewhenbothestimateswereprovidedSecondbecauseestimatesofdivergencetimesdependonthegeneralrateofDNAsubstitutionusedwealsoconsideredtheconfidenceintervalsgen-erated in the studies Lastlywebalanced thequalityof the infor-mationprovidedbyeachstudycaseandthepatterns inferredforlineageswereclassifiedintoldquostrongrdquoorldquomoderaterdquoThusifstudiesprovided divergence time estimates based on phylogenetic rela-tionshipsresolvedwithhigh(iegt90nodalbootstrap)supportfortheECItaxapopulationsthepatternwasclassifiedasldquostrongrdquoBycontrastinferencesweredeemedasldquomoderaterdquoifdivergencewasbasedonlevelsofgeneticdifferentiationandorphylogeneticrecon-structionswithmorelimitedsupport

3emsp |emspSPATIO - TEMPOR AL PAT TERNS

Ourliteraturesurveyallowedidentificationof233plantendemiclin-eages(seeAppendixS1)Wedetectedsomeendemictaxaforwhichassignationtoclearlydefinedislandlineagesisstillhypotheticaldueto the inconclusive information available to date However theseonlyrepresentedasmall fraction(22)ofthetotalOntheotherhandafterexclusionofcasesthatrecentstudieshaveredefinedasendemic or human-introduced native non-endemics were repre-sentedby284lineages

We found significant associations between type of lineage(endemic vs native non-endemic) and extant island distributions(χ2=821plt0001Table2)ThusendemiclineagespreferentiallyoccuronWCI(532ofcases)whereasasmallfractionofthistypeoflineages(c10)isrestrictedtoECI(Table2)Incontrastrecentcolonizers represented by native non-endemic lineages preferen-tially occupy both ECI andWCI (70of the total) and showed asmallnumberofcasesexclusivelyfoundonWCI(158Table2)

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

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ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

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SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

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TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

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SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 6: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

6emsp |emsp emspensp PERSPECTIVE

Divergencetimeestimateswereavailable for42of theen-demic island lineagesbut inclusionofcaseswithmoderatesup-port increased the proportion of endemic lineages up to 54Consideringthesecasesourpredictionsreceiveddifferentlevelsofsupport

31emsp|emspScenario 1 MPT as a temporal filter of dispersal to WCI

Wefoundasubstantialnumberof studiesdealingwithWCI line-agesThisismostprobablyexplainedbytheoverrepresentationofthis type of island distribution among endemicCanarian lineages(Table2)Intotal51studycasessuggestedthatislandcolonizationpredated theonsetof theMPT (P1)while threeadditional casesprovidedmoderatesupportforthisprediction(Figure2)Notablyonlyonestudydocumentedanestimatedageofislandcolonizationwithin theMPT (P2) resulting in a54(P1)1(P2) ratio (i e strongsupportforscenario1)(Figure2)Inmostofthestudieswheredi-vergence time estimates were available confidence intervals didnotoverlapwiththeMPTthresholdwhereasin12othercasesonlya small fractionof theconfidence interval (lt5ndash10)overlappedwithsuchathreshold(Figure3a)Onlythreeislandlineagesshowedestimateddivergencetimesfrommainlandrelativesthatdidnotfallwithin thePliocene-Pleistoceneperiod (meanof estimated islandcolonizationageacrosslineages=39plusmn31MaFigure3a)

32emsp|emspScenario 2 MPT as a disruptor of the progression rule

The number of lineages with ECI-WCI distributions and colo-nization ages older than the onset of theMPT (P3) was higherthan those with younger colonization ages (P4) resulting in a34(P3)15(P4)ratioThesefigureshowevershouldbetakenwithcautionsincewefoundanumberoflineagesforwhichlargecon-fidenceintervalsprecludedunambiguousassignmenttoeitherofthetwopredictions(Figure2)Withinthesetofstudiesprovidingsupport for P3 intra-lineage divergence estimates revealed twocontrastingbiogeographicalpatternsallbuttwolineages(Echium and theAeonium alliance) contained taxa that qualify as recentECIcolonizers(ie95confidenceintervalsvirtuallyoverlappingpresenttimeinallcasesFigure3b)Excludingthesetwolineagesisland colonization times were very recent (08plusmn06Ma acrossECItaxa)ThesefiguresdidnotsupporttheprogressionrulenortheanalysesperformedinthepublishedstudiesrecoveredtheECItaxaasearlydivergentcladesfollowingarchipelagocolonizationIncontrastotherstudiesconductedonlineageswithlimitedtaxo-nomicdifferentiationrevealedyoungcolonizationages(Figure3c)and topological reconstructions among island populations thatwerecongruentwiththeprogressionruleInthesecasescoloni-zationtimesrefertothesplitbetweenmainlandandislandpopula-tionsbutdivergencetimesbetweenECIandWCIpopulationsaretypicallynotreported

33emsp|emspScenario 3 MPT as a driver of recent ECI immigration rates

Wecould not find studies on ECI endemic plant lineages that re-vealedcolonizationagesthatclearlypredatedtheMPTIncontrastthe available information for lineageswith this island distributionprovided21casesofputativerecentorigin(P6Figure2)althoughcolonizationageswereonlyavailableforfiveofthese(meanislandcolonization=05plusmn03MaacrosslineagesFigure3d)TheavailableevidencesuggestshighratesofimmigrationfromcontinentalareassincetheMPT

4emsp |emspHYPOTHESIZED PAT TERNS OF COLONIZ ATION

Takingtheresultsforthesescenariostogetherwehypothesizefivegeneral patterns of island colonization for endemic plant lineageswithafocusontheECI(Table3)

41emsp|emspLineages with extant WCI distributions

MostoftheselineagesareexpectedtohavereachedtheWCIpriortotheMPTThemostplausiblepatternisthattheycolonizedECIbe-foredispersaltoWCIfromwhichtheywentextinctatsomepointThebroadtimespanofislandcolonizationagesinferredforthisisland

TABLE 2emspContingencytableoflineage(endemicvsnativenon-endemic[NativeNE])andislanddistributioncategorieswiththenumberofobservationsfollowedbypercentageofthetotaldata(inparenthesis)DistributionsrepresentingthemostabundantclasswithineachtypeoflineagearehighlightedinboldECI=easternmostislandsWCI=westernislandsECI+WCI=lineagesspanningbothislanddistributions

Lineage

Distribution

TotalWCI ECI+WCI ECI

Endemic 124 (532) 86(369) 23(99) 233

NativeNE 45(158) 199 (701) 40(141) 284

F IGURE 2emspNumberofstudycasesobtainedfromtheliteraturethatsupportseachofthesixpredictionsofourstudy(seeTable1)Blackbarsrepresentstudiesprovidingstrongsupportforeachpredictionwhereasopenbarsrepresentcasesprovidingmoderatesupport

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 7: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp7PERSPECTIVE

distribution (Figure3a) suggests that the hypothetical local extinc-tionfromECImighthaveoccurredatdifferenttimesthroughoutthePlio-PleistoceneHowever theconcentrationof lineageswithcolo-nizationtimeswithinthePleistoceneissuggestiveoffrequentislandextirpationinrecenttimesAlternativepatternssuchasintroductiontotheWCIvianorthernislands(egMadeira)ordirectlong-distancedispersalfromcontinentalareaswouldrepresentanexceptiontothisgeneralcolonizationpattern(ienoneedtoinvokeECIextirpation)

42emsp|emspLineages with extant ECI- WCI distributions

Under the scenario of extinction associated with MPT theprimary spatio-temporal sequence of the progression rule(ie dispersal from mainland to ECI followed by subsequentdispersal toWCI) could occur in the following two cases (a)recent islandcolonizers representedby lineageswith limited

taxonomicdiversificationand (b)oldcolonizing lineagesthatinclude some ECI surviving taxamostly related to the puta-tivePleistocene refugiaof theFamara and Jandiacuteamassifs Inthe latter case lineages with extant ECI-WCI distributionsand colonization times older than the MPT may have expe-rienced extinction of all putative ECI taxa In this particularsubcaseandthecasewhereECIhasexperienceddepaupera-tion back-colonization of ECI fromWCI in recent times canaccount for their current distribution (which may extend toback-colonizationofmainlandareas)

43emsp|emspEndemic lineages to ECI

The available data indicate thatmost of the extant plant lineagesendemic to ECI are the result of recent colonization from conti-nentalareasDispersalfromotherMacaronesianarchipelagos(eg

F IGURE 3emspEstimatedislandcolonizationtimesobtainedfromtheliteratureforCanarianplantlineagesEachestimateisrepresentedwithameanvalue(star)anditsconfidenceinterval(colourbar)Lineagesaredividedintofourclasses(andashd)accordingtotheirextantdistributionsandtaxonomicdiversificationIn(b)estimatesofcolonizationtimesforECItaxaarerepresentedbypurplestarsNumbersnexttoeachestimateidentifyeachlineage(seeAppendixS1)Theextentofthemid-Pleistocenetransitionisrepresentedwithagray-shadedcolumnandmeanvalues(plusmnSD)acrossstudycasesareindicatedforeachlineageclass

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

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Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 8: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

8emsp |emsp emspensp PERSPECTIVE

Madeira Selvagens) to ECIwould represent an alternative sourceareaofsuchrecentcolonizers

5emsp |emspDISCUSSION

51emsp|emspPleistocene extinction as a plausible driver of Quaternary biogeographical patterns in the Canary Islands

OurstudyrevealedtwogeneralpatternsthatarewelldocumentedintheavailableliteratureoftheCanaryIslandflora(a)theoriginofmost island lineages thatareabsent fromtheeasternmost is-landspredatetheonsetoftheMPTand(b)manytaxaendemictotheeasternmostislandsappeartobetheresultofrecent(MPTon-wards)colonizationWithoutfossilevidencetheimpactofextinc-tiononaparticular island lineage ishypothetical (Cardosoetal2010SanmartiacutenampMeseguer2016)Howevertheintersectionofthesetwopatternsandthe jointanalysisofasignificantpropor-tionoftheendemicCanarianfloraallowustodescribeascenarioinwhich Pleistocene extinctionmay have played a fundamentalrole inthefloristicassemblagethatwecurrentlyobserveontheECI

The firstpattern iscongruentwithPleistoceneECIextirpationofextantWCIlineages(Figure3aTable3)anexplanationthathasbeenfrequently hypothesized in biogeographical studies (Arnedo Oromiacuteamp Ribera 2000 Cardoso etal 2010 Vitales etal 2014) In ourstudy comparisons ofmultiple lineages provide an upper bound forthe occurrence of such a phenomenon around the mid-Pleistocene

Notwithstanding the limitations of the approaches for linking diver-gencetimestoislandcolonizationtimes(egPillonampBuerki2017)wearguethatsucharecurrentpatternaddsaplausibleexplanationinad-ditiontodirectdispersaltoWCIfrommainlandforsomeextantspeciesdistributionsThusrecentextinctionofECItaxa(ietimeconstraintsforrecolonization)couldexplainwhyoutstandingexamplesofislandcolo-nizationanddiversificationsuchasCheirolophus(17endemicspecies)or Pericallis (12)havenoextantrepresentativesonthese islandsde-spitepotentialavailabilityofsuitablehabitats(egVitalesetal2014)InturnrecentepisodesofECIcolonization(secondpatternFigure3bTable3)implyearlierextirpationandwouldaccountforthelimitedECIrepresentation(oneortwocloselyrelatedspecies)oflineageswithsim-ilarhighcolonizationabilities(egArgyranthemum SideritisMicromeria)(Curtoetal2017Kimetal2008)

Our study showed that endemic Canarian lineages display astrongbiastowardsWCIdistributionsthussuggestingalargenum-berofcandidatesbeingaffectedbyextirpationWhetherhuman-mediated extinction has a relevant implication in this pattern isuncertainsincewell-documentedcasesofhistoricplantextinctionsarerestrictedtoWCIendemics(deNascimentoetal2009Reyes-Betancort etal 2008) For ECI extirpations apparently derivedfrombackgroundextinctionhabitat loss relatedto islanderosionhasbeenoftensuggestedasthemainexplanatoryfactor(Arnedoetal2000Sanmartiacutenetal2008)However invokingerosionasadriverofextinction implicitlyassumesgeologicalprocessesthatoperateinatime-scaleofMawhichisnotcongruentwiththesec-ondpatternrevealedbyourstudy(ierecentoriginofECIendem-ics)HighimmigrationratesonECI(Figure3bndashd)underlieascenario

TABLE 3emspHypothesizedspatio-temporalpatternsofcolonizationforCanaryislandplantlineagesbasedonextantislanddistributiondegreeoflineagediversification(lowhigh)andislandcolonizationtimeThesepatternsfocusonECIbutmorecomplexscenariosarepossible(seemaintext)Blackcross=totalislandextirpationldquoDottedrdquocross=extinctioncausingbiodiversitydepauperationbutnottotalextinctiononECIDistributionWCI=westernCanaryIslandsECI=easternmostCanaryIslandsM=sourceareasexternaltotheCanaryIslands(egmainlandAfricaMadeira)

Notes(1)Kondraskovetal(2015)(2)Vitalesetal(2014)(3)SunandVargas-Mendoza(2017)(4)Curtoetal(2017)(5)Garciacutea-Marotoetal(2009)(6)Pokornyetal(2015)(7)TalaveraNavarro-SampedroOrtizandArista(2013)(8)Saroetal(2015)(9)Garciacutea-Verdugoetal(2017)(10)BruynsKlakandHanaacuteček(2011)

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 9: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp9PERSPECTIVE

of frequentextinctionwithin the lastmillionofyearsa temporalframe that could hardly imply profound habitat transformationassociatedwith islandontogeny (fora temporal reconstructionoftheislandsseeCaujapeacute-Castellsetal2017)AgaintheimpactofPleistoceneenvironmentalshiftsalbeithypotheticalmaysatisfac-torilyexplainarecentturnoverofterrestrialbiodiversityontheECI(seeegGarciacutea-Aloyetal2017HaaseGreveHuttererampMisof2014)

Theviewof theeasternmost islandsasareasof recentrecolo-nizationquestionstosomeextenttheideaof limitedhabitathet-erogeneityasanexplanatoryfactorfortheirlowendemicrichnessHabitat heterogeneity strongly correlates with species richness(Reyes-Betancortetal2008)andtheECIaregeographicallymorehomogeneousthantheyoungerwesternislandsHoweverseverallinesofevidencesuggestthatthisfactoralonecannotexplaintheirlow endemicity First we found that 70 of extant native non-endemic lineages currently occur on ECI plus another (most fre-quentlyseveral)westernisland(s)(Table2)Thisobservationlinkedwiththehighspeciesdiversityofnon-endemicsfoundontheseis-lands(Figure1d)indicatesthathabitatheterogeneityissufficientlycomplex to act as source (or sink depending on the colonizationroute)ofrecent immigrantstoother islandsSecondseveralareasoftheECIapartfromtheJandiacuteaandFamaramassifs (ieAjachesBetancuriaMontantildeaCardoacutenandCuchillosdeVigaacutenmassifs)couldhaveconsiderably increasedhabitatheterogeneity at leastbeforethe introduction of goats hampered plant population survival inmore recent times Lastly some species of endemicWCI lineagesthathavebeendeliberately introduced to theECI in the last cen-tury (egRumexSalvia) are currently under population expansion(ReyesBetancort1998)whichprovidesevidence thathabitatsofputativelyextirpatedlineagesarenotnecessarilylostWeproposethat limitationsnotstrictlyrelatedtohabitatheterogeneitybuttorecentislandcolonizationmayalsoaccountforthepatternoflowendemicityoftheECI

Our survey identifies a period that rather than a tempo-ral window of colonization (Carine 2005 Kim etal 2008)more specifically appears to have acted as a semi-permeablebarrier of colonization and subsequent speciation Some is-land lineages identified as recent ECI colonizers are com-posed of sister taxa displaying disjunct distributions withinLanzaroteandFuerteventura(ReyesBetancort1998SaacutenchezCaujapeacute-Castells Reyes-Betancort amp Scholz 2006) ThusArgyranthemum Asteriscus Bupleurum and Ferula show pop-ulations mostly confined to the Famara and Jandiacutea massifsThecentral areaofMahanprobably servedasadispersal cor-ridor between both areas during favourable conditions in thePleistocenebutgeographically intermediatepopulationswentextinct probably due toQuaternary climate fluctuations andmore recently to human-related pressures including intensebrowsing by domestic herbivores Such a biogeographicalpattern has been supported by species displaying signaturesof Quaternary population expansion on these islands (JuanIbrahimOromiampHewitt1998SunampVargas-Mendoza2017)

This pattern ultimately reinforces the view of the north andsouthmassifsoftheECIactingasefficientrefugiaandunder-scores geographical isolation as a recent driver of speciationbetweeneasterndisjunctislandpopulations

52emsp|emspHow representative are the proposed colonization patterns of other terrestrial groups

Wewould expect that themain spatio-temporal patterns thatweproposefortheCanarianflora(Table3)shouldbelargelyparalleledbyterrestrialislandelementstightlylinkedwithplantsforexamplehighlyspecializedanimalconsumersAcursoryreviewofthelitera-turepublishedonanimaltaxashowsthatphylogeographicalstudiesoftenretrievecongruentpatternsforspeciesdependentontrophicinteractions (Table4)For instance the idea that lineageswithex-tantWCIdistributionsmayhaveonceoccurredon theeastern is-landsalbeithypotheticalreceivesfurthersupportbythefactthatsomeanimalsandtheirobligateplanthostsappeartodisplayacon-cordantspatio-temporalpattern (Hernaacutendez-TeixidorLoacutepezPonsJuan amp Oromiacute 2016 Percy Page amp Cronk 2004) ColonizationtimesoftheWCIinbothplantandanimalspeciestypicallypredatetheMPT If extinction of former ECI populations is excluded as aplausibleoptionweshouldinvokemultipleeventsofdirectdispersalfromsourceareas toWCI forbothplantandobligateanimal con-sumerswhichseemsunlikelygiventhelargedistancesinvolvedandthelimiteddispersalabilitiesofmostofthesespeciesProgressiveisland hoping followed by Pleistocene extinction on the ECI ap-pears tobe amore likely explanation (eg SauraBodinampFortin2014) Quaternary ECI fossils of gastropod species in the genusThebawhicharecurrentlyrepresentedbyWCIpopulations(Haaseetal2014)alsoprovideinsightsintotheincidenceofPleistoceneextinctionintheislanddistributionsofextantspeciesExamplesofimmigrationofanimal-plant speciespairs toECIeitherasa resultofback-colonizationordispersal frommainlandareas canbealsofoundintheliterature(Table4)andsuggestthatrecentislandcolo-nizationmaybealsomediatedbyfacilitation(BrunoStachowiczampBertness2003)

Furtherevidencefromtheanimalkingdomcomesfromstudiesinferringmultiplecolonizationwavesofconspecifictaxaatdiffer-enttemporalwindowsSucharecurrentpatternofislandcoloniza-tionisintrinsicallyconsistentwiththeideaofextinctionfavouringarrival to islands previously colonized by relatives (Illera etal2016)Inthiscontextplacingextinctionwithinaparticularspatio-temporalbackground(iePleistoceneeasternmostislands)issup-portedbythefactthatECIpopulationsinthesecasesareoftenveryrecent (lt1Ma) (Bidegaray-BatistaTaitiLoacutepez-HernaacutendezRiberaamp Arnedo 2015 Husemann Depperman amp Hochkirch 2014Stervanderetal2015)Thispatternisinagreementwiththosere-vealedbyrecentplantstudiesusingextensivepopulationsamplingofmainlandandislandregions(Garciacutea-Verdugoetal20092017Valtuentildeaetal2016)

In addition some of the patterns receiving limited empiri-cal support from the island plant literaturemay be supplemented

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

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AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

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Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 10: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

10emsp |emsp emspensp PERSPECTIVE

by well-documented cases of animal phylogeography The oldestCanarian islands indeedmay be home of a limited fraction of oldplant lineages (that is thosewhich are hypothesized to have sur-vived inPleistocene refugia)butoursurveyonly found twocaseswithstrongsupport(Aeonium alliance and Echium)Inanimalshow-everthereareseveralspecies-richlineagesinwhichthesignatureofextinctioninsurvivingECI-WCIlineagescanbeinferredfromphy-logenetic(largebranchesandtopologicalbasalposition)anddemo-graphic (Quaternaryeventsofsecondarycladogenesis)approachesdealingwithECItaxa(Bidegaray-BatistaMaciacuteas-HernaacutendezOromiacuteampArnedo 2007 Juan etal 1998) In agreementwith our resultsforAeonium and Echiumitisnoteworthythatanimallineagesqual-ifyingasPleistoceneECIsurvivorsusually includeseveral taxaen-demictoECIWehypothesizethathighECIendemicrichnesswithinagivenlineagemaybeindirectevidenceoftheexpectedeffectsofPleistoceneextinction IfPleistoceneextinctioncausedadramaticreduction in ECI biodiversity levels the processes promoting denovospeciation(iedispersalcolonizationgeographicalecologicalisolation)areprobablytoorecenttohaveallowedtimeformanynewECItaxatoemerge

53emsp|emspImplications for future studies

Modern phylogeographical approaches have increased our abilitytoreconstructcomplexbiogeographicalpatternsbysimultaneouslytestingalternativedemographicscenarios(Curtoetal2017SaroGonzaacutelez-Peacuterez Garciacutea-Verdugo amp Sosa 2015 Sun etal 2016)Assuming the role of Pleistocene extinctions on the ECI providesasetofhypotheseslinkingextant islanddistributionswithtempo-ralwindowsofcolonization (Table3)whichcouldbeeasily imple-mentedinphylogeographicalmodels

Ourfindingsalsoprovideinsightsintotheconservationandtaxon-omyofCanarianplantendemicsFor instance therestricteddistribu-tionofECIendemicscoupledwiththedetrimentaleffectsofintroducedherbivoresanticipateanadversescenarioforlong-termplantsurvivalHowevermostof theECIendemicsmightnotqualify as climate rel-ictsduetotheirputativelyrecentoriginWecouldthusexpectrelativelyquickpopulation recovery inmanycasesprovidedthatperturbationscausedbyintroducedherbivoresaresubstantiallyattenuated Inaddi-tionourstudyhighlightsthatspecieswithWCIdistributionsaretyp-ically associated with old (gt1Ma) colonization times This opens an

TABLE 4emspConcordantphylogeographicalpatternsofplant(P)ndashanimal(A)interactionsobtainedfromindependentstudiesAbbreviationsWCI=westernCanarianislandsECI=easternmostCanarianislandsMPT=mid-Pleistocenetransition

DistributionPtimesA interaction P A Phylogeographical pattern Ref

WCI Obligatehost Euphorbiaspp(Esulasubgen)

Rhopalomesites spp

TheinferredcolonizationtimesforboththeWCIbeetle(32ndash76Ma)andplant(28ndash44)lineagespredatetheMPT

12

WCI Obligatehost Telinespp Arytinnisspp TheinferredcolonizationtimesforboththeWCIlice(c25Ma)andplant(c29Ma)lineagespredatetheMPT

34

WCI-ECI Obligatelarvalhost

Euphorbia regis-jubae

Hyles tithymali BothanimalandplantlineagesinitiallycolonizedthearchipelagobeforetheMPT(gt1Ma)butindependentanalysessuggestWCI-to-ECIcolonizationinveryrecenttimes

567

WCI-ECI Obligatehost Pinus canariensis Brachyderes rugatus

AnalysessuggestthattheonlyknownpopulationofthebeetlelineageonECIistheresultofaveryrecenthuman-mediatedintroductionoftheplanthost

8

WCI-ECI-mainland Obligatehost Euphorbia regis-jubae

Aphanarthrum affine

IndependentstudiesindicateaWCI-ECI-mainlandcolonizationpatternforbothlineagesanddatinganalysesinthehostplantsuggestthatthispatterntookplacewithinthelastMa

97

Mainland-ECI Obligatelarvalhost

Lotus lancerottensis Polyommatus celina

ColonizationtimeofECIfrommainlandinferredforthebutterflyspecies(01ndash03Ma)correspondswiththerecentcolonizationofthehostspecies(00ndash118Ma)

101112

Mainland-ECI Dispersalagent

OleaPhoenixPistacia

SylviasppCorvusTurdus

Recentcolonizationtimeofsomefleshy-fruitedplantlineages(00ndash06Ma)coincideswiththatinferredforthepasserineislandlineagesactingasmaindispersers(00ndash06Ma)

13141516

Notes(1)BarresVilatersanaMoleroSusannaandGalbany-Casals(2011)(2)Hernaacutendez-Teixidoretal(2016)(3)PercyandCronk(2002)(4)Percyetal(2004)(5)HundsdoerferandWink(2006)(6)MendeBartelandHundsdoerfer(2016)(7)Sunetal(2016)(8)Emersonetal(2000)(9)JordalandHewitt(2004)(10)WiemersStradomskyandVodolazhsky(2010)(11)DincăDapportoandVila(2011)(12)Ojedaetal(2014)(13)Saroetal(2015)(14)Nogalesetal(2015)(15)Valenteetal(2017)(16)CGarciacutea-Verdugounpublished

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

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12emsp |emsp emspensp PERSPECTIVE

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CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

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Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

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Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

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deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 11: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp11PERSPECTIVE

interestingvenuefortaxonomicresearchaspopulationsofsomenativenon-endemic taxa currently displaying such distributions could haveevolvedunderisolationforlongertimethanpreviouslythought

6emsp |emspCONCLUSIONS

TheeasternmostislandsofLanzaroteandFuerteventurarepresentabiogeographicalcornerstoneforexplainingpatternsofplantbio-diversityintheCanarianarchipelagoWhiletheiroldvolcanicoriginandclosenesstothecontinentpostulatedthemascradlesofislandbiodiversity they have probably beenmore affected by the con-sequencesof islandontogeny and climatic fluctuations thanmoreisolatedyoungislandsThusourstudysupportsthe ideathattheimpact of Pleistocene extinctions on these islands could explainsome of the recurrent biogeographical patterns described in theregion such as the disruption of the progression rule (Juan etal2000ShawampGillespie2016)ThisscenarioalsoimpliesthattestsofecologicalhypothesesinvolvingtheECIshouldconsiderdetailedphylogeographical information for adequate data interpretation(Garciacutea-Verdugoetal2019MonroyampGarciacutea-Verdugo2019)

TheavailableevidenceindicatesthattheCanaryIslandbiotaisassembled by lineages that colonized the archipelago at differentgeological times but our findings strongly suggest that there is asignificantcomponentofyoung(lt1Ma)plantcolonizersespeciallyontheECISucharelativelyrecentoriginofECIelementsappearstopredateinmostcaseshumanarrivaltotheislands(iebeforethelasttwomillennia)Wethusproposethatconsideringestimatesoflineagecolonizationagesmaybemoreinformativethansurrogatesbasedon islandtraits (iesubaerialages)whentestingforbiogeo-graphicalpredictionsofterrestrialCanariantaxa

Insumwehaveoutlinedaspatio-temporalscenariowhereep-isodesofPleistoceneextinctionmayaccountinadditiontolimitedhabitatheterogeneityfortheuniquepatternsofplantbiodiversityof these islands The peculiar spatial configuration of the CanaryIslands(egECIclosenesstocontinentalmassesandlargeemergedarea)probablymakesourpredictionsoflimitedapplicabilitytomoreisolatedarchipelagoes(egHawaiiGalaacutepagosJuanFernaacutendez)butthe biogeographical consequences anticipated by our conceptualframeworkmightbemirroredbyother terrestrialCanariangroupsandimportantlybylandtaxaoccurringonothernear-shorearchi-pelagos(egRyukyuIzuCaliforniaChannelislands)Furtherstudieswithexplicit assumptionson the imprintofPleistoceneextinctionareneededtodrawageneralpatternofthefactorsaffectingislandterrestrialbiodiversitywithindiscretetemporalscales

ACKNOWLEDG EMENTS

Thedevelopmentof ideas found in thismanuscripthasbeenpos-sible thanks to many contributions made by all those colleagueswho devoted their time to understanding the fascinating biodi-versity of the Macaronesian islands We also appreciate the in-sightful comments provided by three anonymous reviewers for

manuscript improvement C GV was funded by project SV-17-GIJON-BOTANICO JP was funded by theMINECO through theRamoacutenyCajalProgram(RYC-2016-20506)andMarieSklodowska-Curie COFUND Researchers Night and Individual FellowshipsGlobal(MSCAgrantagreementNo747238UNISLAND)

ORCID

Carlos Garciacutea-Verdugo httpsorcidorg0000-0003-0332-5583

Juli Caujapeacute-Castells httpsorcidorg0000-0003-0600-1496

Juan Carlos Illera httpsorcidorg0000-0002-4389-0264

Mario Mairal httpsorcidorg0000-0002-6588-5634

Jairo Patintildeo httpsorcidorg0000-0001-5532-166X

KeywordsbackgroundextinctioncolonizationpatternsglacialrefugiaislandbiogeographyMahanPleistoceneclimaticshifts

CarlosGarciacutea-Verdugo1

JuliCaujapeacute-Castells2

JuanCarlosIllera3

MarioMairal4

JairoPatintildeo56

AlfredoReyes-Betancort7

StephanScholz8

1Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de Oviedo GijoacutenXixoacuten Spain2Departamento de Biodiversidad Molecular y Banco de ADN Jardiacuten

Botaacutenico Canario lsquoViera y Clavijorsquo ndash Unidad Asociada CSIC Cabildo de Gran Canaria Las Palmas de Gran Canaria Spain

3Unidad Mixta de Investigacioacuten en Biodiversidad (UO-CSIC-PA) Oviedo University Mieres Spain

4Department of Botany and Zoology Stellenbosch University Matieland South Africa

5Plant Conservation and Biogeography Group Departamento de Botaacutenica Ecologiacutea y Fisiologiacutea Vegetal Universidad de La Laguna La

Laguna Tenerife Spain6Island Ecology and Evolution Research Group Instituto de Productos

Naturales y Agrobiologiacutea (IPNA-CSIC) La Laguna Tenerife Spain7Jardiacuten de Aclimatacioacuten de la Orotava (ICIA) Puerto de la Cruz SC de

Tenerife Spain8Oasis Park Fuerteventura Paacutejara Spain

CorrespondenceCarlos Garciacutea-Verdugo Jardiacuten Botaacutenico Atlaacutentico ndash Universidad de

Oviedo GijoacutenXixoacuten SpainEmail carlosgarciaverdugogmailcom

Editor Dr Hanno Schaefer

R E FE R E N C E S

AcebesJRLeoacutenMCRodriacuteguezNavarroMLdelArcoMGarciacuteaGalloAdePeacuterezPazPLhellipWildpretW(2010)Pteridophytaspermato-phytaInMArechavaletaSRodriacuteguezNZuritaampAGarciacutea(Eds)Lista

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

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Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

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14emsp |emsp emspensp PERSPECTIVE

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Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

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MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

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PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

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Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 12: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

12emsp |emsp emspensp PERSPECTIVE

de especies silvestres de Canarias Hongos plantas y animales terrestres 2009(pp119ndash172)SantaCruzdeTenerifeSpainGobiernodeCanarias

Aedo C Medina L Barberaacute P amp Fernaacutendez-Albert M (2015)ExtinctionsofvascularplantsinSpainNordic Journal of Botany31478ndash488

AndersonCLChanningAampZamunerAB(2009)Lifedeathandfossilization on Gran Canaria ndashimplications forMacaronesian bio-geographyandmoleculardatingJournal of Biogeography362189ndash2201httpsdoiorg101111j1365-2699200902222x

ArnedoMAOromiacutePampRiberaC(2000)SystematicsofthegenusDysdera (Araneae Dysderidae) in the eastern Canary Islands The Journal of Arachnology28261ndash292httpsdoiorg1016360161-8202(2000)028[0261SOTGDA]20CO2

BarresLVilatersanaRMoleroJSusannaAampGalbany-CasalsM(2011)MolecularphylogenyofEuphorbia subgEsula sectAphyllis (Euphorbiaceae)inferredfromnrDNAandcpDNAmarkerswithbio-geographic insights Taxon 60 705ndash720 httpsdoiorg101002tax603007

BellemainEampRicklefsRE(2008)Areislandstheendofthecoloni-zationroadTrends in Ecology and Evolution23461ndash468httpsdoiorg101016jtree200805001

Bidegaray-Batista L Maciacuteas-Hernaacutendez N E Oromiacute P amp ArnedoM A (2007) Living on the edge Demographic and phylo-geographic patterns in the woodlousehunter spider Dysdera lancerotensis Simon 1907 on the eastern volcanic ridge of theCanary Islands Molecular Ecology 16 3198ndash3214 httpsdoiorg101111j1365-294X200703351x

Bidegaray-Batista L Taiti S Loacutepez-Hernaacutendez H Ribera C ampArnedoMA(2015)Endemismandevolutioninthelittoralwood-louseHalophilosciaVerhoeff1908 (Crustacea IsopodaOniscidea)from the Canary Islands Implications for conservation policiesInsect Conservation and Diversity817ndash30httpsdoiorg101111icad12079

Bramwell D (1976) The endemic flora of the Canary Islands dis-tribution relationships and phytogeography In G Kunkel (Ed)Biogeography and ecology in the Canary Islands (pp 207ndash240) TheHagueTheNetherlandsJunkhttpsdoiorg101007978-94-010- 1566-0

Brodie J F Aslan C E Rogers H S Redford K H Maron J LBronsteire J L ampGroves C R (2014) Secondary extinctions ofbiodiversityTrends in Ecology and Evolution29664ndash672httpsdoiorg101016jtree201409012

BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169-5347(02)00045-9

Bruyns PV KlakCampHanaacuteček P (2011)Age anddiversity inOldWorld succulent species of Euphorbia (Euphorbiaceae) Taxon 601717ndash1733httpsdoiorg101002tax606016

BurnsKC(2018)Timetoabandonthelossofdispersalabilityhypoth-esisinislandplantsAcommentonGarciacutea-VerdugoMairalMonroySajeva and Caujapeacute-Castells (2017) Journal of Biogeography 451219ndash1222httpsdoiorg101111jbi13223

CardosoPArnedoMTriantisKAampBorgesPAV(2010)Driversof diversity in Macaronesian spiders and the role of species ex-tinctions Journal of Biogeography 37 1034ndash1046 httpsdoiorg101111j1365-2699200902264x

CarineMA(2005)Spatio-temporalrelationshipsoftheMacaronesianendemicfloraArelictualseriesorwindowofopportunityTaxon54895ndash903httpsdoiorg10230725065476

CarlquistSJ(1974)Island biologyNewYorkNYColumbiaUniversityPresshttpsdoiorg105962bhltitle63768

Caujapeacute-Castells J (2004) Boomerangs of biodiversity The inter-changeofbiodiversitybetweenmainlandNorthAfricaandtheCanaryIslands as inferred from cpDNA RFLPs in genus Androcymbium Botaacutenica Macaroneacutesica2553ndash69

Caujapeacute-Castells J Garciacutea-Verdugo C Marrero-Rodriacuteguez AFernaacutendez-PalaciosJMCrawfordDJampMortME(2017)Islandontogeniessyngameonsandtheoriginsandevolutionofgeneticdi-versity in theCanarianendemic floraPerspectives in Plant Ecology Evolution and Systematics 27 9ndash22 httpsdoiorg101016jppees201703003

CodyMLampMcOvertonJM(1996)Short-termevolutionofreduceddispersal in islandplantpopulations Journal of Ecology84 53ndash61httpsdoiorg1023072261699

Condamine F L Leslie A B amp Antonelli A (2017) Ancient islandsactedasrefugiaandpumpsforconiferdiversityCladistics3369ndash92httpsdoiorg101111cla12155

Cronk Q C B (1997) Islands Stability diversity conserva-tion Biodiversity and Conservation 6 477ndash493 httpsdoiorg101023A1018372910025

CurtoMPuppoPKratschmerSampMeimbergH(2017)Geneticdi-versityanddifferentiationpatterns inMicromeria from theCanaryIslandsarecongruentwithmultiplecolonizationdynamicsand theestablishmentofspeciessyngameonsBMC Evolutionary Biology17198httpsdoiorg101186s12862-017-1031-y

deNascimentoLWillisKJFernaacutendez-PalaciosJMCriadoCampWhittaker R J (2009) The long-term ecology of the lost forestsofLaLagunaTenerife(CanaryIslands)Journal of Biogeography36499ndash514httpsdoiorg101111j1365-2699200802012x

DeacutesamoreacuteA LaenenBDevosN PoppMGonzaacutelez-Mancebo JMCarineMAampVanderpoortenA(2011)OutofAfricaNorth-westwardsPleistoceneexpansionsoftheheatherErica arborea Journal of Biogeography38 164ndash176httpsdoiorg101111j1365-2699 201002387x

Dincă V Dapporto L amp Vila R (2011) A combined genetic-morphometric analysis unravels the complex biogeographicalhistory of Polyommatus icarus and Polyommatus celina CommonBlue butterflies Molecular Ecology 20 3921ndash3935 httpsdoiorg101111j1365-294X201105223x

EmersonBC(2002)EvolutiononoceanicislandsMolecularphylogeneticapproachestounderstandingpatternandprocessMolecular Ecology11951ndash966httpsdoiorg101046j1365-294X200201507x

EmersonBC(2003)GenesgeologyandbiodiversityFaunalandflo-ral diversity on the islandofGranCanariaAnimal Biodiversity and Conservation269ndash20

EmersonBCOromiPampHewittG(2000)Colonisationanddiversifi-cationofthespeciesBrachyderes rugatus(Coleoptera)ontheCanaryIslands Evidence from mitochondrial DNA COII gene sequencesEvolution54 911ndash923 httpsdoiorg101111j0014-38202000tb00091x

Erwin D M amp Schorn H E (2000) Revision of Lyonothamnus A Gray(Rosaceae) from theNeogeneofwesternNorthAmerica International Journal of Plant Sciences161179ndash193httpsdoiorg101086314232

Fernaacutendez-Palacios J M de Nascimento L Otto R Delgado JD Garciacutea del Rey E Areacutevalo J R amp Whittaker R J (2011)A reconstruction of Palaeo-Macaronesia with particular refer-ence to the long-term biogeography of the Atlantic island lau-rel forests Journal of Biogeography 38 226ndash246 httpsdoiorg101111j1365-2699201002427x

Fernaacutendez-Palacios J M Rijsdijk K F Norder S J Otto R deNascimentoLFernaacutendez-LugoShellipWhittakerRJ(2016)Towardsa glacial-sensitive model of island biogeographyGlobal Ecology and Biogeography25817ndash830httpsdoiorg101111geb12320

Franzke A Sharif Samani B R Neuffer B Mummenhoff K ampHurka H (2017) Molecular evidence in Diplotaxis (Brassicaceae)suggests a Quaternary origin of the Cape Verdean flora Plant Systematics and Evolution 303 467ndash479 httpsdoiorg101007s00606-016-1384-5

Gangoso L Donaacutezar J A Scholz S Palacios C amp Hiraldo F(2006) Contradiction in conservation of island ecosystems

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 13: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp13PERSPECTIVE

Plants introduced herbivores and avian scavengers in the CanaryIslands Biodiversity and Conservation 15 2231ndash2248 httpsdoiorg101007s10531-004-7181-4

Garciacutea-AloySVitalesDRoquetCSanmartiacutenIVargasPMoleroJhellipAlarcoacutenM (2017)North-westAfricaasasourceandrefugeareaofplantbiodiversityA case studyonCampanula kremeri and Campanula occidentalis Journal of Biogeography 44 2057ndash2068httpsdoiorg101111jbi12997

Garciacutea-Maroto F Mantildeas-Fernaacutendez A Garrido-Caacuterdenas J ALoacutepez-Alonso D Guil-Guerrero J L Guzmaacuten B amp Vargas P(2009) D6-Desaturase sequence evidence for explosive Plioceneradiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)Molecular Phylogenetics and Evolution52 563ndash574httpsdoiorg101016jympev200904009

Garciacutea-Verdugo C Baldwin B G Fay M F amp Caujapeacute-Castells J(2014)Lifehistorytraitsandpatternsofdiversificationinoceanicar-chipelagosAmeta-analysisBotanical Journal of the Linnean Society174334ndash348httpsdoiorg101111boj12127

Garciacutea-Verdugo C Calleja J A Vargas P Silva L Moreira O ampPulidoF(2013)PolyploidyandmicrosatellitevariationintherelicttreePrunus lusitanicaLHoweffectivearerefugiainpreservingge-notypicdiversityofclonal taxaMolecular Ecology221546ndash1557httpsdoiorg101111mec12194

Garciacutea-VerdugoCCaujapeacute-CastellsJMairalMampMonroyP(2019)Howrepeatable ismicroevolutionon islandsPatternsofdispersaland colonization-related plant traits in a phylogeographical con-textAnnals of Botany123 557ndash568httpsdoiorg101093aobmcy191

Garciacutea-Verdugo C Fay M F Granado-Yela C Rubio de CasasR Balaguer L Besnard G amp Vargas P (2009) Genetic di-versity and differentiation processes in the ploidy series ofOlea europaea A multiscale approach from subspecies to is-land populations Molecular Ecology 18 454ndash467 httpsdoiorg101111j1365-294X200804027x

Garciacutea-Verdugo C Mairal M Monroy P Sajeva M amp Caujapeacute-CastellsJ(2017)Thelossofdispersalonislandshypothesisrevis-ited Implementingphylogeography to investigateevolutionofdis-persaltraitsinPeriploca(Apocynaceae)Journal of Biogeography442595ndash2606httpsdoiorg101111jbi13050

GeniseJFampEdwardsN(2003)Ichnotaxonomyoriginandpaleoenvi-ronmentofQuaternaryinsectcellsfromFuerteventuraCanaryIslandsSpainJournal of the Kansas Entomological Society76320ndash327

GibsonLACowanMALyonsMNPalmerRPearsonDJampDoughty P (2017) Island refuges Conservation significance ofthe biodiversity patterns resulting from lsquonaturalrsquo fragmentationBiological Conservation 212 349ndash356 httpsdoiorg101016jbiocon201706010

GillespieRGampClagueDA(2009)Encyclopedia of islandsBerkeleyCAUniversityofCaliforniaPress

HaaseMGreveCHuttererRampMisofB(2014)Amplifiedfragmentlengthpolymorphisms theevolutionof the landsnailgenusTheba (StylommatophoraHelicidae)andanobjectiveapproach for relat-ingfossilsto internalnodesofaphylogenetictreeusinggeometricmorphometricsZoological Journal of the Linnean Society17192ndash107httpsdoiorg101111zoj12123

HardieDCampHutchingsJA(2010)Evolutionaryecologyattheex-tremesofspeciesrsquorangesEnvironmental Reviews181ndash20httpsdoiorg101139A09-014

Hernaacutendez-TeixidorDLoacutepezHPonsJJuanCampOromiacuteP(2016)Host plant associations and geographical factors in the diversifi-cation of the Macaronesian Rhopalomesites beetles (ColeopteraCurculionidae) Journal of Biogeography431608ndash1619httpsdoiorg101111jbi12737

Hundsdoerfer A K amp Wink M (2006) Incongruence of mor-phology and genetic markers in Hyles tithymali (Lepidoptera

Sphingidae) from the Canary Islands Journal of Zoological Systematics and Evolutionary Research 44 316ndash322 httpsdoiorg101111j1439-0469200600366x

HusemannMDeppermanJampHochkirchA(2014)Multipleinde-pendentcolonizationof theCanary Islandsby thewingedgrass-hopper genusSphingonotus Fieber 1852Molecular Phylogenetics and Evolution 81 174ndash181 httpsdoiorg101016jympev201409017

Hutsemeacutekers V Szoumlveacutenyi P Shaw A J Gonzaacutelez-Mancebo J MMuntildeozJampVanderpoortenA(2011)Oceanicislandsarenotsinksofbiodiversityinspore-producingplantsProceedings of the National Academy of Sciences of the USA10818989ndash18994

Illera J C Diacuteaz M amp Nogales M (2006) Ecological traits in-fluence the current distribution and range of an island en-demic bird Journal of Biogeography 33 1192ndash1201 httpsdoiorg101111j1365-2699200601505x

IlleraJCSpurginLGRodriguez-ExpositoENogalesMampRandoJC(2016)Whatarewelearningaboutspeciationandextinctionfromthe Canary Islands Ardeola 63 15ndash33 httpsdoiorg1013157arla6312016rp1

JanssonR (2003)Globalpatterns inendemismexplainedbypastcli-maticchangeProceedings of the Royal Society B Biological Sciences270583ndash590httpsdoiorg101098rspb20022283

JonesKEReyes-BetancortJAHiscockSJampCarineMA(2014)Allopatricdiversificationmultiplehabitatshiftsandancienthybrid-iationintheevolutionofPericallis(Asteraceae)American Journal of Botany1011ndash15

Jordal B H amp Hewitt G M (2004) The origin and radiation ofMacaronesian beetles breeding in Euphorbia The relative impor-tanceofmultipledatapartitionsandpopulationsamplingSystematic Biology53711ndash734httpsdoiorg10108010635150490468710

JuanCEmersonBCOromiacutePampHewittGM(2000)Colonizationand diversification Towards a phylogeographic synthesis for theCanary IslandsTrends in Ecology amp Evolution15 104ndash109httpsdoiorg101016S0169-5347(99)01776-0

JuanCIbrahimKOromiPampHewittGM(1998)Thephylogeog-raphyof thedarklingbeetleHegeter politus in theeasternCanaryIslandsProceedings of the Royal Society of London Series B265135ndash140httpsdoiorg101098rspb19980274

Kier G Kreft H Lee T M Jetz W Ibisch P L Nowicki C hellipBarthlott W (2009) A global assessment of endemism and spe-ciesrichnessacross islandandmainlandregionsProceedings of the National Academy of Sciences USA 106 9322ndash9327 httpsdoiorg101073pnas0810306106

KimS-CMcGowenMRLubinskyPBarberJMortMampSantos-GuerraA(2008)TimingandtempoofearlyandsuccessiveadaptiveradiationsinMacaronesiaPLoS ONE31ndash7

Kondraskov P Schuumltz N Schuumlszligler C Menezes de SequeiraM Santos-Guerra A Caujapeacute-Castells J hellip Thiv M (2015)Biogeography of Mediterranean hotspot biodiversity Re-evaluating the lsquoTertiaryRelictrsquo hypothesis ofMacaronesian laurelforestsPLoS ONE10e0132091httpsdoiorg101371journalpone0132091

KunkelG(Ed)(1976)Biogeography and ecology in the Canary IslandsTheHagueTheNetherlandsDrWJunkPublishers

Loulergue L Schilt A Spahni R Masson-Delmotte V Blunier TLemieuxBhellipChappellazJ(2008)Orbitalandmillennial-scalefea-turesofatmosphericCH4overthepast800000yearsNature453383ndash386httpsdoiorg101038nature06950

LoweJJampWalkerMJC(2015)Reconstructing Quaternary environ-ments(3rded)NewYorkNYRoutledge

MacArthurRHampWilsonEO(1967)The theory of island biogeogra-phyPrincetonNJPrincetonUniversityPress

MarreroAampFrancisco-OrtegaJ (2001)Evolucioacutenen islas lametaacute-fora espacio-tiempo-forma In J M Fernaacutendez-Palacios amp J L

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 14: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

14emsp |emsp emspensp PERSPECTIVE

Martiacuten-Esquivel (Eds) Naturaleza de las Islas Canarias Ecologiacutea y Conservacioacuten(pp133ndash140)MadridSpainPublicacionesTurquesaSL

Meco J Petit-MaireNGuillouHCarracedo JC LomoschitzARamos A J G amp Ballester J (2003) Climatic changes over thelast5000000yearsasrecordedintheCanaryIslandsEpisodes6133ndash134

MeacutedailFampQueacutezelP(1999)ThephytogeographicalsignificanceofSWMoroccocomparedtotheCanary IslandsPlant Ecology140221ndash244httpsdoiorg101023A1009775327616

MendeMBBartelMampHundsdoerferAK (2016)Acomprehen-sivephylogeographyof theHyles euphorbiae complex (LepidopteraSphingidae) indicates a lsquoglacial refuge beltrsquo Scientific Reports 629527httpsdoiorg101038srep29527

MonroyPampGarciacutea-VerdugoC(2019)TestingthehypothesisoflossofdefencesonislandsacrossawidelatitudinalgradientofPeriploca laevigata populations American Journal of Botany 106 303ndash312httpsdoiorg101002ajb21232

NogalesMHelenoR RumeuBGonzaacutelez-CastroA TravesetAVargasPampOlensenJM(2015)Seed-dispersalnetworksontheCanariesandtheGalapagosarchipelagosInteractionmodulesasbio-geographicalentitiesGlobal Ecology and Biogeography25912ndash922

Norder S J Proios KWhittaker R J AlonsoM R Borges P ABorregaardMKhellipKisslingWD(2019)BeyondtheLastGlacialMaximumIslandendemismisbestexplainedby long-lastingarchi-pelagoconfigurationsGlobal Ecology and Biogeography28184ndash197httpsdoiorg101111geb12835

OjedaDISantos-GuerraAOliva-TejeraFJaen-MolinaRCaujapeacute-CastellsJMarrero-RodriacuteguezAampCronkQ(2014)DNAbarcodessuccessfully identified Macaronesian Lotus (Leguminosae) specieswithinearlydiverged lineagesofCapeVerdeandmainlandAfricaAoB PLANTS6plu050httpsdoiorg101093aobplaplu050

OrtizJETorresTYanesYCastilloCdelaNuezJIbaacutentildeezMampAlonsoMR (2006)Climaticcycles inferredfromaminostratigra-phyandaminochronologyofQuaternarydunesandpalaeosolsfromtheeasternislandsoftheCanaryArchipelagoJournal of Quaternary Science21287ndash306httpsdoiorg101002(ISSN)1099-1417

PatintildeoJCarineMAMardulynPDevosNMateoRGGonzaacutelez-ManceboJMhellipVanderpoortenA(2015)ApproximateBayesiancomputationrevealsthecrucialroleofoceanicislandsfortheassem-blyofcontinentalbiodiversitySystematic Biology64579ndash589

PercyDMampCronkQCB(2002)DifferentfatesofislandbroomsContrastingevolutioninAdenocarpus Genista and Teline(GenisteaeFabaceae) in the Canary Islands andMadeiraAmerican Journal of Botany89854ndash864httpsdoiorg103732ajb895854

PercyDMPageRDMampCronkQCB (2004)Plant-insect in-teractionsDouble-datingassociatedinsectandplantlineagerevealsasynchrous radiationsSystematic Biology53120ndash127httpsdoiorg10108010635150490264996

PillonYampBuerki S (2017)Howold are island endemicsBiological Journal of the Linnean Society121469ndash474httpsdoiorg101093biolinneanblx005

PokornyLRiinaRMairalMMeseguerASCulshawVCendoyaJhellipSanmartiacutenI(2015)LivingontheedgeTimingofRandFloradisjunctionscongruentwithongoingaridificationinAfricaFrontiers in Genetics6154

Prebble M Whitau R Meyer J-Y Sibley-Punnett L Fallon S ampPorchN(2016)LatePleistoceneecologicalandclimatechangeonTahiti (French Polynesia) Journal of Biogeography 43 2438ndash2453httpsdoiorg101111jbi12807

PriceJPOttoRdeSequeiraMMKuefferCSchaeferHCaujapeacute-CastellsJampFernaacutendez-PalaciosJM(2018)Colonizationanddi-versificationshapespeciesndasharearelationshipsinthreeMacaronesianarchipelagos Journal of Biogeography 45 2027ndash2039 httpsdoiorg101111jbi13396

ReyesBetancortJA(1998)Flora y Vegetacioacuten de la isla de Lanzarote (res-erva de la Biosfera)PhDthesisDptodeBiologiacuteaVegetal-UniversidaddeLaLaguna

Reyes-BetancortASantos-GuerraAGumaRHumphriesCJampCarineM(2008)DiversityrarityandtheevolutionandconservationoftheCanaryIslandsendemicfloraAnales del Jardiacuten Botaacutenico de Madrid6525ndash45

Rodriacuteguez Rodriacuteguez A Mora J L Arbelo C amp Bordon J (2005)Plant succession and soil degradation in desertified areas(FuerteventuraCanaryIslandsSpain)Catena59117ndash131httpsdoiorg101016jcatena200407002

Rodriguez-SanchezFampArroyoJ(2008)ReconstructingthedemiseofTethyanplantsClimate-driven rangedynamicsofLaurus since thePlioceneGlobal Ecology and Biogeography17685ndash695httpsdoiorg101111j1466-8238200800410x

SaacutenchezJLCaujapeacute-CastellsJReyes-BetancortJAampScholzS(2006)Population genetic variation of Matthiola bolleana Webb ex Christ(Brassicaceae)anendemictotheeasternCanaryIslandsofFuerteventuraandLanzarotePlant Systematics and Evolution262139ndash151

SanmartiacutenIampMeseguerAS(2016)Extinctioninphylogeneticsandbio-geographyFromtimetreestopatternsofbioticassemblageFrontiers in Genetics71ndash17

Sanmartiacuten I van der Mark P amp Ronquist F (2008) Inferringdispersal A Bayesian approach to phylogeny-based is-land biogeography with special reference to the CanaryIslands Journal of Biogeography 35 428ndash449 httpsdoiorg101111j1365-2699200801885x

Saro IGonzaacutelez-PeacuterezMAGarciacutea-VerdugoCamp Sosa PA (2015)PatternsofgeneticdiversityinPhoenix canariensisawidespreadoce-anicpalm(species)endemicfromtheCanarianarchipelagoTree Genetics and Genomes11815httpsdoiorg101007s11295-014-0815-0

SauerJD(1969)OceanicislandsandbiogeographicaltheoryAreviewGeographical Review59582ndash593httpsdoiorg102307213863

SauraSBodinOumlampFortinM-J (2014)Steppingstonesarecrucialfor speciesrsquo long-distance dispersal and range expansion throughhabitatnetworksJournal of Applied Ecology51171ndash182httpsdoiorg1011111365-266412179

ShawK LampGillespie RG (2016)Comparative phylogeographyofoceanicarchipelagosHotspots for inferencesofevolutionarypro-cessProceedings of the National Academy of Sciences USA1137986ndash7993httpsdoiorg101073pnas1601078113

SilvertownJ(2004)Theghostofcompetitionpastinthephylogenyofisland endemic plants Journal of Ecology92 168ndash173 httpsdoiorg101111j1365-2745200400853x

Stervander M Illera J C Kvist L Barbosa P Keehnen N PPruisscherPhellipHanssonB(2015)Disentanglingthecomplexevo-lutionaryhistoryofthewesternPalearcticbluetits(Cyanistesspp)ndashphylogenomicanalysessuggestradiationbymultiplecolonizationeventsandsubsequentisolationMolecular Ecology242477ndash2494httpsdoiorg101111mec13145

SunYLiYSVargas-MendozaCFWangFGampXingFW(2016)Colonization and diversification of the Euphorbia species (SectAphyllis subsect Macaronesicae) on the Canary Islands Scientific Reports634454httpsdoiorg101038srep34454

SunYampVargas-MendozaCF (2017)Population structuregeneticdiversity and evolutionary history ofKleinia neriifolia (Asteraceae)ontheCanaryIslandsFrontiers in Plant Science81180httpsdoiorg103389fpls201701180

Talavera M Navarro-Sampedro L Ortiz P L amp Arista M (2013)Phylogeography and seed dispersal in islands The case of Rumex bucephalophorussubspcanariensis(Polygonaceae)Annals of Botany111249ndash260httpsdoiorg101093aobmcs284

TerzopoulouSRigalFWhittakerRJBorgesPAampTriantisKA(2015)DriversofextinctionThecaseofAzoreanbeetlesBiology Letters1120150273httpsdoiorg101098rsbl20150273

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563

Page 15: Pleistocene extinctions as drivers of biogeographical ... · that Pleistocene extinctions may have significantly eachcontributed to extant biogeographical patterns in Neuffer,the

emspensp emsp | emsp15PERSPECTIVE

Valente L Illera J C Havenstein K Pallien T Etienne R S ampTiedemannR (2017)Equilibriumbirdspeciesdiversity inAtlanticislands Current Biology 27 1660ndash1666 httpsdoiorg101016jcub201704053

Valtuentildea F J Loacutepez J Alvarez J Rodriacuteguez-Riantildeo T amp Ortega-OlivenciaA(2016)Scrophularia argutaawidespreadannualplantintheCanaryIslandsAsinglerecentcolonizationeventoramorecom-plexphylogeographicpatternEcology and Evolution64258ndash4273httpsdoiorg101002ece32109

Vargas P (2007) Are Macaronesian islands refugia of relict plantlineages A molecular survey In S Weiss amp N Ferrand (Eds)Phylogeography of Southern European refugia ndash Evolutionary perspec-tives on the origins and conservation of European biodiversity(pp297ndash341)TheHagueSpringer

Vitales D Garnatje T Pellicer J Vallegraves J Santos-Guerra A ampSanmartiacuten I (2014) The explosive radiation of Cheirolophus (Asteraceae Cardueae) in Macaronesia BMC Evolutionary Biology14118httpsdoiorg1011861471-2148-14-118

WeigeltPSteinbauerMJSarmentoCabralJampKreftH(2016)LateQuaternaryclimatechangeshapes islandbiodiversityNature53299ndash102httpsdoiorg101038nature17443

WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography OxfordUKOxfordUniversityPress

WhittakerRJTriantisKAampLadleRJ(2008)Ageneraldynamictheoryofoceanic islandbiogeography Journal of Biogeography35977ndash994httpsdoiorg101111j1365-2699200801892x

WiemersMStradomskyBVampVodolazhskyDI(2010)AmolecularphylogenyofPolyommatussstrandPlebiculabasedonmitochondrialCOIandnuclearITS2sequences(LepidopteraLycaenidae)European Journal of Entomology 107 325ndash336 httpsdoiorg1014411eje2010041

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleGarciacutea-VerdugoCCaujapeacute-CastellsJIlleraJCetalPleistoceneextinctionsasdriversofbiogeographicalpatternsontheeasternmostCanaryIslandsJ Biogeogr 2019001ndash15 httpsdoiorg101111jbi13563


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