R E S E A R CH P A P E R
The roles of dispersal and mass extinction in shaping palmdiversity across the Caribbean
Angela Cano12 | Christine D Bacon23 | Fred W Stauffer1 |
Alexandre Antonelli234 | Martha L Serrano-Serrano5 | Mathieu Perret1
1Conservatoire et Jardin botaniques de la
Ville de Geneve and Department of Botany
and Plant Biology University of Geneva
Chambesy Geneva Switzerland
2Gothenburg Global Biodiversity Centre
Geurooteborg Sweden
3Department of Biological and
Environmental Sciences University of
Gothenburg Geurooteborg Sweden
4Gothenburg Botanical Garden Geurooteborg
Sweden
5Department of Ecology and Evolution
University of Lausanne Lausanne
Switzerland
CorrespondenceAngela Cano Conservatoire et Jardin
botaniques de la Ville de Geneve Chambesy
Geneva Switzerland
Email angelacano11gmailcom
Funding information
European Research Council GrantAward
Number 331024 Vetenskapsradet Grant
Award Number B0569601 Swiss National
Science Foundation GrantAward Number
31003A_1756551
Editor Lyn Cook
Abstract
Aim The rich flora of the Caribbean islands and surrounding mainland evolved in a
context of isolation alternated with phases of terrestrial connectivity between land-
masses climatic fluctuations and episodes of mass extinctions during the Cenozoic
We explored how these events affected the evolution of the sister palm tribes
Cryosophileae and Sabaleae and how continent-island exchanges endemic radia-
tions and mass extinction shaped their extant diversity
Location The American continent including the Caribbean region
Methods We reconstructed a time-calibrated phylogeny of the palm tribes Cryoso-
phileae and Sabaleae using 84 of the known species We inferred ancestral distri-
bution and tested the effect of island colonization and mass extinction on extant
diversity
Results Our results indicate that Cryosophileae and Sabaleae originated c 77 Ma
most probably in Laurasia and their extant species started to diversify between 56ndash
35 Ma and 19ndash10 Ma respectively Biogeographical state reconstruction estimated
that Cryosophileae dispersed to South America between 56ndash35 Ma then dispersed to
North-Central America between 39ndash25 Ma and the Caribbean islands between 34ndash
21 Ma We detected a possible signature of a mass extinction event at the end of the
Eocene affecting the diversification of Cryosophileae and Sabaleae and we did not
detect a diversification rate shift related to the colonization of the Caribbean islands
Main conclusions Species of Cryosophileae in the Caribbean islands are probably
derived from a single Oligocene dispersal event that likely occurred overwater from
North-Central America rather than through the hypothesized GAARlandia land
bridge Contrastingly three independent Miocene dispersal events from North-Cen-
tral America explain the occurrence of Sabaleae in the Caribbean islands Contrary
to our expectations island colonization did not trigger increased diversification
Instead we find that diversification patterns in this clade and its disappearance
from northernmost latitudes could be the signature of a mass extinction triggered
by the global temperature decline at the end of the Eocene
K E YWORD S
Arecaceae Boreotropical migrations Caribbean Coryphoideae diversification mass extinction
overwater dispersal palms Sabal West Indies
DOI 101111jbi13225
Journal of Biogeography 20181ndash12 wileyonlinelibrarycomjournaljbi copy 2018 John Wiley amp Sons Ltd | 1
1 | INTRODUCTION
The Americas have experienced dramatic geological changes over
the past 100 Myr North America was temporarily connected to Eur-
asia through the North Atlantic and Beringian land bridges (Brikiatis
2014 and references therein) Central America was hit by a massive
meteorite (Schulte et al 2010) the Caribbean islands emerged and
drifted eastwards in the Caribbean Sea (Iturralde-Vinent amp MacPhee
1999) and South America ended its isolation with the formation of
the Panama Isthmus (Montes et al 2015) How these events influ-
enced the outstanding biodiversity of the Neotropics has been a
subject of long-standing discussion (Antonelli amp Sanmartın 2011a)
renewed in recent years with the advent of new molecular dating
and biogeographical methods and cross-taxonomic comparative
analyses (eg Bacon et al 2015 Hoorn et al 2010 OrsquoDea et al
2016 Rull 2011) In this context the Andean and Amazonian
regions have drawn the most attention while much less effort has
been devoted to understanding the evolution of the Caribbean in
particular its flora
The sister palm tribes Cryosophileae and Sabaleae (subfamily
Coryphoideae) known as the New World Thatch Palms (NWTP
Dransfield et al 2008) have evolved in the dynamic context of the
Caribbean They are currently restricted to the Caribbean islands (34
species most of them in the Greater Antilles) and nearby landmasses
of North-Central America (25 species) and South America (10 spe-
cies) (Henderson Galeano amp Bernal 1995) However they had a lar-
ger past distribution in the Northern hemisphere as evidenced by
their extensive fossil record (Figure 1) that dates to the Late Creta-
ceous (Manchester Lehman amp Wheeler 2010) Combining these
fossil data with a phylogeny of extant NWTP species would help
retrace their evolution in time and space and illuminate the origin
and diversification of the Caribbean flora
The Caribbean region including the Greater and Lesser Antilles
contains about 13000 seed plant species Of these 72 are ende-
mic to the region and at least 10 are either endangered or critically
endangered sensu the International Union for Conservation of Nat-
ure (Acevedo-Rodrıguez amp Strong 2008 Oleas et al 2013) Com-
parative studies have shown a floristic affinity between the
Caribbean islands and the surrounding mainland (Acevedo-Rodrıguez
amp Strong 2008) but our understanding of the underlying evolution-
ary processes that shaped this diversity is still limited (Francisco-
Ortega et al 2007 Graham 2003 Nieto-Blazquez Antonelli amp
Roncal 2017 Santiago-Valentin amp Olmstead 2004) Available bio-
geographical studies focused on Caribbean plants point to multiple
biotic exchanges among the islands between North-Central America
and South America and local diversifications (Cervantes Fuentes
Gutierrez Magallon amp Borsch 2016 van Ee Berry Riina amp
Gutierrez Amaro 2008 Santiago-Valentin amp Olmstead 2004) For
example the Caribbean Acalyphoideae (Euphorbiaceae) are esti-
mated to have repeatedly colonized the Caribbean islands during the
Miocene mainly from Central America (Cervantes et al 2016)
whereas Brunfelsia (Solanaceae) probably entered the Antilles 8ndash
6 Ma from South America (Filipowicz amp Renner 2012) Phylogenetic
studies in different palm lineages also indicate independent coloniza-
tions of the Caribbean islands from the mainland and multiple migra-
tions between North and South America (Bacon Baker amp Simmons
2012 Bacon Mora Wagner amp Jaramillo 2013 Cuenca Asmussen-
Lange amp Borchsenius 2008 Roncal Zona amp Lewis 2008) For the
NWTP previous phylogenetic hypotheses have suggested an origin
of the Caribbean taxa from a mainland ancestor (Roncal et al 2008)
However a better resolved phylogeny is needed to trace whether
their diversity in the Caribbean is the result of multiple mainland-
island dispersal events or a colonization event followed by local
diversification
Several geological models have been hypothesized to facilitate
interchanges between land areas around the Caribbean region These
include the Proto-Antilles connecting North to South America during
the Late Cretaceous to the Palaeocene (94ndash63 Ma Graham 2003)
the Greater Antilles-Aves Ridge (GAARlandia) connecting the West
Indies to South America during the Oligocene (35ndash33 Ma Iturralde-
F IGURE 1 Distribution of extant Cryosophileae and Sabaleae (pink area) and fossils related to them from different epochs Late Cretaceous(black 100ndash66 Ma) Paleogene (grey 66ndash23 Ma) Neogene (white 23ndash26 Ma) Shapes represent different taxonomic groups triangleCryosophileae square Sabal circle Sabalites See Appendix S1 for data sources Map projection sphere Mollweide (53009)
2 | CANO ET AL
Vinent amp MacPhee 1999) and the Panama Isthmus formation start-
ing in the Miocene (Montes et al 2015) To what extent these puta-
tive corridors facilitated species dispersal across the Caribbean
region is still debated (eg Ali 2012 Nieto-Blazquez et al 2017)
and several studies postulate that overwater dispersal events have
played a major role in the biogeographical history of Caribbean plant
lineages (Cervantes et al 2016 Gugger amp Cavender-Bares 2013)
In addition to dispersal the dynamics of speciation and extinc-
tion during the history of lineages may also have influenced the cur-
rent patterns of species richness across the Caribbean and
surrounding areas (Ricklefs amp Bermingham 2008) The colonization
of archipelagos has been frequently associated with an increase of
morphological and taxonomic diversity (Bacon et al 2012 Baldwin
amp Sanderson 1998 Condamine Leslie amp Antonelli 2016 Losos amp
Ricklefs 2009) The diversification rate shift estimated for the Carib-
bean Coccothrinax (Baker amp Couvreur 2013b) the most diverse
genus of the NWTP is congruent with the hypothesis of a species
radiation triggered by island colonization Alternatively mass extinc-
tion events could also have influenced how diversity accumulated
through time (Antonelli amp Sanmartın 2011b Brocklehurst Ruta
Meurouller amp Freuroobisch 2015 Crisp amp Cook 2009) In particular three
episodes of relatively rapid climatic cooling could have affected the
diversity of frost-intolerant plants in the Caribbean region (1) the
CretaceousndashPalaeogene Event (66 Ma) when a large meteorite
impacted the Yucatan Peninsula generating immediate global dark-
ness and cooling (Schulte et al 2010) (2) the Terminal Eocene
Event (35 Ma) when global temperatures drastically dropped nega-
tively affecting the Boreotropical flora that covered large parts of
Laurasia (Morley 2003) and (3) the period following the mid-Mio-
cene climatic optimum (12 Ma) when globally warm equable cli-
mates shifted to present-day cooler and more seasonal climates
(Zachos Dickens amp Zeebe 2008) It remains unclear if the NWTP
which are considered typical elements of the Boreotropical flora
(Bjorholm Svenning Baker Skov amp Balslev 2006) were more
affected by Cenozoic cooling that caused their extirpation from Eur-
asia and northern North America (Figure 1) or by the meteorite
impact in the vicinity of their distribution range
We generated a time-calibrated species phylogeny of the NWTP
and used it to infer the biogeographical scenario that best explains
their current distribution and diversity We addressed the following
specific questions (1) When and where did the NWTP originate (2)
Is their diversity in the Caribbean the result of one or multiple dis-
persal events and which colonization routes did they follow (3)
How did island colonization and global episodes of mass extinction
influence extant NWTP diversity across the Caribbean and surround-
ing areas
2 | MATERIALS AND METHODS
21 | Taxon sampling
Our sampling includes 89 accessions from 67 species Sampling in
Cryosophileae (11 genera 35 species of 42) is complete except in
the genera Cryosophila (7 species of 10 sensu Evans 1995) and Coc-
cothrinax (10 species of 14 sensu Henderson et al 1995) Sampling
in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe-
cies of Sabal (Dransfield et al 2008) To evaluate the phylogenetic
position of the NWTP within Coryphoideae we also sampled repre-
sentatives of other tribes in this subfamily Two outgroups were
selected in subfamilies Ceroxyloideae and Arecoideae Silica-gel dried
leaf fragments were collected in the field (collection and export per-
mits 111296 and 113458 respectively from the Paraguayan Secre-
tarıa del Ambiente) or in the living collections of the Conservatoire et
Jardin botaniques de la Ville de Geneve (Switzerland) Montgomery
Botanical Center Fairchild Tropical Botanical Garden (both in the
USA) and the Jardın Botanico del Quindıo (Colombia) Voucher infor-
mation is provided in Table S11 (see Appendix S1 in Supporting
Information)
22 | Phylogenetic analyses
Four nuclear (CISP4 CISP5 PRK and RPB2) and one plastid (matK)
loci were sequenced following the protocol described in
Appendix S1 and using the primers listed in Table S12 The DNA
sequences are deposited in GenBank under the accession numbers
listed in Table S11 Sequences were aligned using MAFFT 7130
(Katoh Misawa Kuma amp Miyata 2002) Sites were scored with
GUIDANCE 141 (Penn et al 2010) and excluded from further analy-
ses if their score was lt08 to avoid adding noise to the branch
length and substitution rate estimates (Jordan amp Goldman 2012)
The final database contained 4872 bp Phylogenetic analyses were
performed on the CIPRES portal (Miller Pfeiffer amp Schwartz 2010)
Single-gene and combined partitioned phylogenetic analyses were
carried out with MRBAYES 322 (Ronquist et al 2012) In the parti-
tioned analyses the dataset was divided into five partitions corre-
sponding to each marker The best fitting substitution model for
each partition was selected from 24 models with MRAICPL 146
(Nylander 2004) using the Akaike information criterion (AIC) The
test selected the models HKY for CISP4 CISP5 and PRK GTR for
matK and GTR+Γ for RPB2 Four Markov chains were run for
5 9 106 generations with a heating temperature of 015 Samples
were logged every 100th generation Using TRACER 16 (Rambaut
Suchard Xie amp Drummond 2014) we determined burnin (24) and
confirmed trace stationarity and sufficient sampling (effective sample
size [ESS] gt200)
23 | Fossil calibration and divergence time analyses
Three fossils were used to estimate divergence times (Table S13)
Following Couvreur Forest and Baker (2011) fossils of Sabalites
carolinensis Berry and Hyphaene kappelmanii Pan et al were used to
constrain the stem nodes of subfamily Coryphoideae and subtribe
Hyphaeninae (Coryphoideae) respectively In addition fossilized
seeds of Sabal bigbendense (Manchester et al 2010) were used to
calibrate the stem node of Sabaleae These seeds from the Late Cre-
taceous (c 77 Ma) represent the oldest record attributed to the
CANO ET AL | 3
tribe Since the use of this fossil for calibrating the NWTPrsquos phy-
logeny has a strong effect on the divergence time estimates (Fig-
ure S11) a close evaluation of its relationship with the extant genus
Sabal was conducted and its classification within Sabaleae was sup-
ported (Appendix S1)
Divergence time analyses were conducted in BEAST 180 (Drum-
mond Suchard Xie amp Rambaut 2012) applying the same partitions
and substitution models as for MRBAYES Substitution and clock mod-
els were set as unlinked whereas tree models were linked among
partitions Clock model tests using stepping-stone sampling (SSS)
and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured
a relaxed clock with an uncorrelated lognormal distribution (UCLN
marginal log-likelihood = 2364194 BF = 111167) against a strict
clock (marginal log-likelihood = 2419777) We used uniform distri-
butions for UCLN mean priors for each data partition with default
initial and lower values and upper values set to 100 To assess the
impact of tree-model selection on our divergence time estimations
we compared the median node ages obtained with a Yule versus a
BirthndashDeath process model The differences ranged from 010 to
225 Ma and were markedly smaller than the 95 HPD age bars for
each model (Figure S12) indicating that both tree models yield simi-
lar divergence time estimations Because tree-model tests strongly
favoured a Yule Process (marginal log-likelihood = 2364194
BF = 7165) over a BirthndashDeath process (marginal log-
likelihood = 2367776) the Yule tree model was implemented in
further analyses
To account for uncertainty in fossil dating and identification
soft-bound lognormal priors were used for all calibration points with
standard deviations set such that 95 of the age distribution fell
within the geological time period of the fossil stratigraphic source
(Table S13 Yang amp Rannala 2006) Seven independent chains were
run for 50 9 106 generations sampling every 10000th generation
All the chains converged and their ESS values were above 200
Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-
TOR 180 (Drummond et al 2012) was used to exclude the adequate
proportion of burnin samples and obtain a maximum clade credibility
(MCC) tree displaying median heights
24 | Biogeographical analyses
Five biogeographical areas were defined (O) Old World (N) North-
Central America (S) South America (I) Panama Isthmus delimited
between the El Valle area (Panama) and the Uramita suture
(Colombia Montes et al 2015) and (C) Caribbean islands The lat-
ter were treated as a single area to facilitate understanding of bio-
tic exchanges amongst insular-continental regions A distinction
between the Greater and the Lesser Antilles was not appropriate
since most of the NWTP species occur in the Greater Antilles (34
species) and only two widespread species are present in the Lesser
Antilles Species distributions were compiled from the literature
(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans
1995 Henderson et al 1995 Zona 1990) and from the Global
Biodiversity Information Facility (GBIF httpwwwgbiforg
accessed 17 July 2014) Conflicting occurrences from GBIF (eg
palms cultivated in botanic gardens) were excluded
We inferred the biogeographical history of the NWTP using the
Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)
model (Ree amp Smith 2008) with and without the parameter ldquojrdquo
accounting for the probability of founder-event speciation as imple-
mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The
DEC+j model is appropriate in this study since the NWTP occur in
areas that have been isolated (South America the Caribbean islands)
and therefore instantaneous speciation in conjunction with long-dis-
tance dispersal may be expected Analyses were applied to the MCC
tree and tree uncertainty was considered for the interpretation of
results The tree was pruned to include a single terminal per species
The maximum number of areas at nodes was restricted to three to
simplify the computational effort and because three is the maximum
number of areas currently inhabited by any NWTP species Analyses
were conducted with and without dispersal constraints Dispersal
constraints (Table S14) were applied by assigning different dispersal
probabilities as follows p = 1 for dispersal between adjacent areas
p = 5 for dispersal over the Caribbean Sea or through non-adjacent
land areas (eg between N and S) and p = 01 for dispersal over the
Atlantic Ocean (eg between S and O) or across the fully formed
Northern Andes barrier As a sensitivity test to parameter choice
when the lowest dispersal probability was set to 01 instead of 001
no significant differences were found in the biogeographical recon-
struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141
lnL difference lt2 log-likelihood units) and relative probabilities (Fig-
ure S13)
Four time periods were defined (1) 90ndash33 Ma probability of dis-
persal from areas O to N through the Beringian and North Atlantic
land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the
Northern Hemisphere were no longer available (Brikiatis 2014) (3)
15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)
7 Ma-present final uplift of the Northern Andes acting as a barrier
for dispersal between Amazonia and Choco (Luebert amp Weiged
2014 Table S15)
25 | Diversification analyses
We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the
existence (if any) and number of diversification rate shifts in the
NWTP phylogeny A set of 120 trees were randomly chosen from
the BEAST sampling to calculate maximum likelihood estimates of spe-
ciation and extinction rates and rate shift times The function
bdshiftsoptimum was set to optimize the model parameters in 100
iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma
(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect
[Nee Holmes May amp Harvey 1994]) To determine how many rate
shifts are most probable given the phylogenies models with n and
n + 1 shifts were compared with likelihood ratio tests following the
greedy approach by Stadler (2011a) Mean and standard deviation of
diversification rates and shift ages were calculated across the 120
trees
4 | CANO ET AL
To evaluate whether shifts in diversification rate could be attrib-
uted to a specific clade we used BAMM 20 (Rabosky 2014
Appendix S2) Controversy exists regarding the adequacy of BAMM
for diversification rate inference (Moore Hohna May Rannala amp
Huelsenbeck 2016) However recent evaluations of the method
suggested that diversification rate inference with BAMM is accurate
and consistent (Rabosky Mitchell amp Chang 2017) We used the
extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-
age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether
the colonization of the Caribbean islands was associated with shifts
in diversification rates (Appendix S2)
Finally to explore whether the temporal gap between stem and
crown ages observed in the NWTP phylogeny could be the signature
of mass extinction instead of low diversification followed by recent
radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-
dler 2011b) Following the approach by Antonelli and Sanmartın
(2011b) the shapes and the ages of Lineage Through Time (LTT)
curves of simulated trees were compared to the LTT curve observed
for the crown NWTP MCC tree Three sets of simulations were run
with the function simrateshifttaxa where only 5 of the lineages
survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-
minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)
In all sets the speciation (0223) and extinction (0180) rates were
kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200
trees were simulated to reflect stochastic variance with a final num-
ber of 54 terminals (the number of terminals in the crown NWTP
MCC tree) and accounting for the missing taxa with frac = 093
3 | RESULTS
31 | Phylogenetic analyses
The analyses of four independent loci support the sister relationship
between the tribes Cryosophileae and Sabaleae (posterior probability
[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister
in the CISP4 gene tree (Figure S21) but the alternative relationships
are not supported (PP lt 090) The comparison of individual gene
trees did not reveal other topological incongruences with PP gt095
MRBAYES and BEAST analyses of the combined partitioned dataset
recovered congruent results and the MCC tree from BEAST is shown
in Figure 2
32 | Divergence time and ancestral rangeestimation
Calibration analyses (Figure 2) inferred crown ages for the NWTP in
the Late Cretaceous (77 Ma [age values correspond to median
heights estimated with BEAST] 787ndash761 Ma [age ranges correspond
to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the
Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene
(14 Ma 187ndash96 Ma)
The most likely biogeographical model was DEC+j with dispersal
constraints (lnL = 914 Figure 3a) followed with a difference of
42 log-likelihood units by DEC with dispersal constraints
(lnL = 956) and by DEC+j without dispersal constraints
(lnL = 1024) Biogeographical analyses indicate that the NWTP
most probably originated in North America (pC = 045) sometime
during the Late Cretaceous By the Eocene Cryosophileae dispersed
to South America (pS = 067) giving rise to the genera Chelyocarpus
Itaya Sabinaria and Trithrinax Later during the early Oligocene
members of Cryosophileae dispersed back to North-Central America
and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)
Sabaleae most probably started diversifying in an area encompassing
both North America and the Caribbean islands (pNC = 050) or only
in North America (pN = 046) Two unambiguous dispersal events
from the continent to the Caribbean islands were inferred between
15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)
33 | Diversification analyses
A likelihood ratio test indicated that a model accounting for one rate
shift was strongly supported against a model without rate shifts
(mean p = 99 Table S21) Models with two or more rate shifts did
not improve model fit Figure 3b shows the mean diversification rate
as a function of time with 80 confidence interval across the 120
trees sampled A diversification rate shift was estimated around
108 Ma (SD = 80) Mean diversification rates were
0012 0014 Ma1 before the rate shift and 015 005 Ma1
after it No significant rate shifts were detected in specific branches
of the MCC tree (Figure S26) and diversification rate in Caribbean
lineages was not significantly different from that of continental
clades (Appendix S2)
Most of the trees simulated with a mass extinction occurring
66 Ma did not display the broom-and-handle shape of the empirical
tree and the crown ages of these trees were younger than the
crown NWTP age (Figure 4a median crown age 47 Ma range of
crown ages 1667ndash191 Ma) The majority of the trees simulated
under a mass extinction 35 Ma displayed the same broom-and-han-
dle shape as our empirical crown NWTP tree (Figure 4b) the crown
age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within
the lower quartile of crown ages of simulated trees which ranged
from 2039 to 218 Ma (median crown age 103 Ma) Most of the
trees simulated with a mass extinction occurring 12 Ma did not dis-
play the broom-and-handle shape of the empirical tree and their
crown ages were older than the crown NWTP age (Figure 4c med-
ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)
4 | DISCUSSION
41 | Divergence times and historical biogeography
411 | Origin of the NWTP in time and space
With all genera and 84 of species sampled our MCC tree (Fig-
ure 2) constitutes the most complete phylogenetic hypothesis
assembled to date for the NWTP Our results are congruent with
CANO ET AL | 5
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
REFERENCES
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oiorg101007s12229-008-9000-1
Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-
cal and simulated approaches Systematic Biology 60 596ndash615
httpsdoiorg101093sysbiosyr062
Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
National Academy of Sciences 108 8379ndash8384 httpsdoiorg10
1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
drives island radiations in the palm tribe Trachycarpeae (Arecaceae)
Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
geological models of evolution of the Isthmus of Panama in a phylo-
genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
plex emergence of the Isthmus of Panama Proceedings of the National
Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas
1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages I Historical biogeography Journal of Biogeography 40 274ndash
285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
of the Hawaiian silversword alliance (Compositae) Proceedings of the
National Academy of Sciences 95 9402ndash9406 httpsdoiorg10
1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
Chave J (2013) Origin and evolution of Chrysobalanaceae Insights
into the evolution of plants in the Neotropics Botanical Journal of the
Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339
201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-
der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
Society 151 113ndash125 httpsdoiorg101111j1095-83392006
00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
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graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
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Stadler T (2011a) Mammalian phylogeny reveals recent diversification
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cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
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Miocene of France) Anatomy palaeobiogeography and evolutionary
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httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
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oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
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Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
1 | INTRODUCTION
The Americas have experienced dramatic geological changes over
the past 100 Myr North America was temporarily connected to Eur-
asia through the North Atlantic and Beringian land bridges (Brikiatis
2014 and references therein) Central America was hit by a massive
meteorite (Schulte et al 2010) the Caribbean islands emerged and
drifted eastwards in the Caribbean Sea (Iturralde-Vinent amp MacPhee
1999) and South America ended its isolation with the formation of
the Panama Isthmus (Montes et al 2015) How these events influ-
enced the outstanding biodiversity of the Neotropics has been a
subject of long-standing discussion (Antonelli amp Sanmartın 2011a)
renewed in recent years with the advent of new molecular dating
and biogeographical methods and cross-taxonomic comparative
analyses (eg Bacon et al 2015 Hoorn et al 2010 OrsquoDea et al
2016 Rull 2011) In this context the Andean and Amazonian
regions have drawn the most attention while much less effort has
been devoted to understanding the evolution of the Caribbean in
particular its flora
The sister palm tribes Cryosophileae and Sabaleae (subfamily
Coryphoideae) known as the New World Thatch Palms (NWTP
Dransfield et al 2008) have evolved in the dynamic context of the
Caribbean They are currently restricted to the Caribbean islands (34
species most of them in the Greater Antilles) and nearby landmasses
of North-Central America (25 species) and South America (10 spe-
cies) (Henderson Galeano amp Bernal 1995) However they had a lar-
ger past distribution in the Northern hemisphere as evidenced by
their extensive fossil record (Figure 1) that dates to the Late Creta-
ceous (Manchester Lehman amp Wheeler 2010) Combining these
fossil data with a phylogeny of extant NWTP species would help
retrace their evolution in time and space and illuminate the origin
and diversification of the Caribbean flora
The Caribbean region including the Greater and Lesser Antilles
contains about 13000 seed plant species Of these 72 are ende-
mic to the region and at least 10 are either endangered or critically
endangered sensu the International Union for Conservation of Nat-
ure (Acevedo-Rodrıguez amp Strong 2008 Oleas et al 2013) Com-
parative studies have shown a floristic affinity between the
Caribbean islands and the surrounding mainland (Acevedo-Rodrıguez
amp Strong 2008) but our understanding of the underlying evolution-
ary processes that shaped this diversity is still limited (Francisco-
Ortega et al 2007 Graham 2003 Nieto-Blazquez Antonelli amp
Roncal 2017 Santiago-Valentin amp Olmstead 2004) Available bio-
geographical studies focused on Caribbean plants point to multiple
biotic exchanges among the islands between North-Central America
and South America and local diversifications (Cervantes Fuentes
Gutierrez Magallon amp Borsch 2016 van Ee Berry Riina amp
Gutierrez Amaro 2008 Santiago-Valentin amp Olmstead 2004) For
example the Caribbean Acalyphoideae (Euphorbiaceae) are esti-
mated to have repeatedly colonized the Caribbean islands during the
Miocene mainly from Central America (Cervantes et al 2016)
whereas Brunfelsia (Solanaceae) probably entered the Antilles 8ndash
6 Ma from South America (Filipowicz amp Renner 2012) Phylogenetic
studies in different palm lineages also indicate independent coloniza-
tions of the Caribbean islands from the mainland and multiple migra-
tions between North and South America (Bacon Baker amp Simmons
2012 Bacon Mora Wagner amp Jaramillo 2013 Cuenca Asmussen-
Lange amp Borchsenius 2008 Roncal Zona amp Lewis 2008) For the
NWTP previous phylogenetic hypotheses have suggested an origin
of the Caribbean taxa from a mainland ancestor (Roncal et al 2008)
However a better resolved phylogeny is needed to trace whether
their diversity in the Caribbean is the result of multiple mainland-
island dispersal events or a colonization event followed by local
diversification
Several geological models have been hypothesized to facilitate
interchanges between land areas around the Caribbean region These
include the Proto-Antilles connecting North to South America during
the Late Cretaceous to the Palaeocene (94ndash63 Ma Graham 2003)
the Greater Antilles-Aves Ridge (GAARlandia) connecting the West
Indies to South America during the Oligocene (35ndash33 Ma Iturralde-
F IGURE 1 Distribution of extant Cryosophileae and Sabaleae (pink area) and fossils related to them from different epochs Late Cretaceous(black 100ndash66 Ma) Paleogene (grey 66ndash23 Ma) Neogene (white 23ndash26 Ma) Shapes represent different taxonomic groups triangleCryosophileae square Sabal circle Sabalites See Appendix S1 for data sources Map projection sphere Mollweide (53009)
2 | CANO ET AL
Vinent amp MacPhee 1999) and the Panama Isthmus formation start-
ing in the Miocene (Montes et al 2015) To what extent these puta-
tive corridors facilitated species dispersal across the Caribbean
region is still debated (eg Ali 2012 Nieto-Blazquez et al 2017)
and several studies postulate that overwater dispersal events have
played a major role in the biogeographical history of Caribbean plant
lineages (Cervantes et al 2016 Gugger amp Cavender-Bares 2013)
In addition to dispersal the dynamics of speciation and extinc-
tion during the history of lineages may also have influenced the cur-
rent patterns of species richness across the Caribbean and
surrounding areas (Ricklefs amp Bermingham 2008) The colonization
of archipelagos has been frequently associated with an increase of
morphological and taxonomic diversity (Bacon et al 2012 Baldwin
amp Sanderson 1998 Condamine Leslie amp Antonelli 2016 Losos amp
Ricklefs 2009) The diversification rate shift estimated for the Carib-
bean Coccothrinax (Baker amp Couvreur 2013b) the most diverse
genus of the NWTP is congruent with the hypothesis of a species
radiation triggered by island colonization Alternatively mass extinc-
tion events could also have influenced how diversity accumulated
through time (Antonelli amp Sanmartın 2011b Brocklehurst Ruta
Meurouller amp Freuroobisch 2015 Crisp amp Cook 2009) In particular three
episodes of relatively rapid climatic cooling could have affected the
diversity of frost-intolerant plants in the Caribbean region (1) the
CretaceousndashPalaeogene Event (66 Ma) when a large meteorite
impacted the Yucatan Peninsula generating immediate global dark-
ness and cooling (Schulte et al 2010) (2) the Terminal Eocene
Event (35 Ma) when global temperatures drastically dropped nega-
tively affecting the Boreotropical flora that covered large parts of
Laurasia (Morley 2003) and (3) the period following the mid-Mio-
cene climatic optimum (12 Ma) when globally warm equable cli-
mates shifted to present-day cooler and more seasonal climates
(Zachos Dickens amp Zeebe 2008) It remains unclear if the NWTP
which are considered typical elements of the Boreotropical flora
(Bjorholm Svenning Baker Skov amp Balslev 2006) were more
affected by Cenozoic cooling that caused their extirpation from Eur-
asia and northern North America (Figure 1) or by the meteorite
impact in the vicinity of their distribution range
We generated a time-calibrated species phylogeny of the NWTP
and used it to infer the biogeographical scenario that best explains
their current distribution and diversity We addressed the following
specific questions (1) When and where did the NWTP originate (2)
Is their diversity in the Caribbean the result of one or multiple dis-
persal events and which colonization routes did they follow (3)
How did island colonization and global episodes of mass extinction
influence extant NWTP diversity across the Caribbean and surround-
ing areas
2 | MATERIALS AND METHODS
21 | Taxon sampling
Our sampling includes 89 accessions from 67 species Sampling in
Cryosophileae (11 genera 35 species of 42) is complete except in
the genera Cryosophila (7 species of 10 sensu Evans 1995) and Coc-
cothrinax (10 species of 14 sensu Henderson et al 1995) Sampling
in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe-
cies of Sabal (Dransfield et al 2008) To evaluate the phylogenetic
position of the NWTP within Coryphoideae we also sampled repre-
sentatives of other tribes in this subfamily Two outgroups were
selected in subfamilies Ceroxyloideae and Arecoideae Silica-gel dried
leaf fragments were collected in the field (collection and export per-
mits 111296 and 113458 respectively from the Paraguayan Secre-
tarıa del Ambiente) or in the living collections of the Conservatoire et
Jardin botaniques de la Ville de Geneve (Switzerland) Montgomery
Botanical Center Fairchild Tropical Botanical Garden (both in the
USA) and the Jardın Botanico del Quindıo (Colombia) Voucher infor-
mation is provided in Table S11 (see Appendix S1 in Supporting
Information)
22 | Phylogenetic analyses
Four nuclear (CISP4 CISP5 PRK and RPB2) and one plastid (matK)
loci were sequenced following the protocol described in
Appendix S1 and using the primers listed in Table S12 The DNA
sequences are deposited in GenBank under the accession numbers
listed in Table S11 Sequences were aligned using MAFFT 7130
(Katoh Misawa Kuma amp Miyata 2002) Sites were scored with
GUIDANCE 141 (Penn et al 2010) and excluded from further analy-
ses if their score was lt08 to avoid adding noise to the branch
length and substitution rate estimates (Jordan amp Goldman 2012)
The final database contained 4872 bp Phylogenetic analyses were
performed on the CIPRES portal (Miller Pfeiffer amp Schwartz 2010)
Single-gene and combined partitioned phylogenetic analyses were
carried out with MRBAYES 322 (Ronquist et al 2012) In the parti-
tioned analyses the dataset was divided into five partitions corre-
sponding to each marker The best fitting substitution model for
each partition was selected from 24 models with MRAICPL 146
(Nylander 2004) using the Akaike information criterion (AIC) The
test selected the models HKY for CISP4 CISP5 and PRK GTR for
matK and GTR+Γ for RPB2 Four Markov chains were run for
5 9 106 generations with a heating temperature of 015 Samples
were logged every 100th generation Using TRACER 16 (Rambaut
Suchard Xie amp Drummond 2014) we determined burnin (24) and
confirmed trace stationarity and sufficient sampling (effective sample
size [ESS] gt200)
23 | Fossil calibration and divergence time analyses
Three fossils were used to estimate divergence times (Table S13)
Following Couvreur Forest and Baker (2011) fossils of Sabalites
carolinensis Berry and Hyphaene kappelmanii Pan et al were used to
constrain the stem nodes of subfamily Coryphoideae and subtribe
Hyphaeninae (Coryphoideae) respectively In addition fossilized
seeds of Sabal bigbendense (Manchester et al 2010) were used to
calibrate the stem node of Sabaleae These seeds from the Late Cre-
taceous (c 77 Ma) represent the oldest record attributed to the
CANO ET AL | 3
tribe Since the use of this fossil for calibrating the NWTPrsquos phy-
logeny has a strong effect on the divergence time estimates (Fig-
ure S11) a close evaluation of its relationship with the extant genus
Sabal was conducted and its classification within Sabaleae was sup-
ported (Appendix S1)
Divergence time analyses were conducted in BEAST 180 (Drum-
mond Suchard Xie amp Rambaut 2012) applying the same partitions
and substitution models as for MRBAYES Substitution and clock mod-
els were set as unlinked whereas tree models were linked among
partitions Clock model tests using stepping-stone sampling (SSS)
and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured
a relaxed clock with an uncorrelated lognormal distribution (UCLN
marginal log-likelihood = 2364194 BF = 111167) against a strict
clock (marginal log-likelihood = 2419777) We used uniform distri-
butions for UCLN mean priors for each data partition with default
initial and lower values and upper values set to 100 To assess the
impact of tree-model selection on our divergence time estimations
we compared the median node ages obtained with a Yule versus a
BirthndashDeath process model The differences ranged from 010 to
225 Ma and were markedly smaller than the 95 HPD age bars for
each model (Figure S12) indicating that both tree models yield simi-
lar divergence time estimations Because tree-model tests strongly
favoured a Yule Process (marginal log-likelihood = 2364194
BF = 7165) over a BirthndashDeath process (marginal log-
likelihood = 2367776) the Yule tree model was implemented in
further analyses
To account for uncertainty in fossil dating and identification
soft-bound lognormal priors were used for all calibration points with
standard deviations set such that 95 of the age distribution fell
within the geological time period of the fossil stratigraphic source
(Table S13 Yang amp Rannala 2006) Seven independent chains were
run for 50 9 106 generations sampling every 10000th generation
All the chains converged and their ESS values were above 200
Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-
TOR 180 (Drummond et al 2012) was used to exclude the adequate
proportion of burnin samples and obtain a maximum clade credibility
(MCC) tree displaying median heights
24 | Biogeographical analyses
Five biogeographical areas were defined (O) Old World (N) North-
Central America (S) South America (I) Panama Isthmus delimited
between the El Valle area (Panama) and the Uramita suture
(Colombia Montes et al 2015) and (C) Caribbean islands The lat-
ter were treated as a single area to facilitate understanding of bio-
tic exchanges amongst insular-continental regions A distinction
between the Greater and the Lesser Antilles was not appropriate
since most of the NWTP species occur in the Greater Antilles (34
species) and only two widespread species are present in the Lesser
Antilles Species distributions were compiled from the literature
(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans
1995 Henderson et al 1995 Zona 1990) and from the Global
Biodiversity Information Facility (GBIF httpwwwgbiforg
accessed 17 July 2014) Conflicting occurrences from GBIF (eg
palms cultivated in botanic gardens) were excluded
We inferred the biogeographical history of the NWTP using the
Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)
model (Ree amp Smith 2008) with and without the parameter ldquojrdquo
accounting for the probability of founder-event speciation as imple-
mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The
DEC+j model is appropriate in this study since the NWTP occur in
areas that have been isolated (South America the Caribbean islands)
and therefore instantaneous speciation in conjunction with long-dis-
tance dispersal may be expected Analyses were applied to the MCC
tree and tree uncertainty was considered for the interpretation of
results The tree was pruned to include a single terminal per species
The maximum number of areas at nodes was restricted to three to
simplify the computational effort and because three is the maximum
number of areas currently inhabited by any NWTP species Analyses
were conducted with and without dispersal constraints Dispersal
constraints (Table S14) were applied by assigning different dispersal
probabilities as follows p = 1 for dispersal between adjacent areas
p = 5 for dispersal over the Caribbean Sea or through non-adjacent
land areas (eg between N and S) and p = 01 for dispersal over the
Atlantic Ocean (eg between S and O) or across the fully formed
Northern Andes barrier As a sensitivity test to parameter choice
when the lowest dispersal probability was set to 01 instead of 001
no significant differences were found in the biogeographical recon-
struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141
lnL difference lt2 log-likelihood units) and relative probabilities (Fig-
ure S13)
Four time periods were defined (1) 90ndash33 Ma probability of dis-
persal from areas O to N through the Beringian and North Atlantic
land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the
Northern Hemisphere were no longer available (Brikiatis 2014) (3)
15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)
7 Ma-present final uplift of the Northern Andes acting as a barrier
for dispersal between Amazonia and Choco (Luebert amp Weiged
2014 Table S15)
25 | Diversification analyses
We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the
existence (if any) and number of diversification rate shifts in the
NWTP phylogeny A set of 120 trees were randomly chosen from
the BEAST sampling to calculate maximum likelihood estimates of spe-
ciation and extinction rates and rate shift times The function
bdshiftsoptimum was set to optimize the model parameters in 100
iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma
(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect
[Nee Holmes May amp Harvey 1994]) To determine how many rate
shifts are most probable given the phylogenies models with n and
n + 1 shifts were compared with likelihood ratio tests following the
greedy approach by Stadler (2011a) Mean and standard deviation of
diversification rates and shift ages were calculated across the 120
trees
4 | CANO ET AL
To evaluate whether shifts in diversification rate could be attrib-
uted to a specific clade we used BAMM 20 (Rabosky 2014
Appendix S2) Controversy exists regarding the adequacy of BAMM
for diversification rate inference (Moore Hohna May Rannala amp
Huelsenbeck 2016) However recent evaluations of the method
suggested that diversification rate inference with BAMM is accurate
and consistent (Rabosky Mitchell amp Chang 2017) We used the
extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-
age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether
the colonization of the Caribbean islands was associated with shifts
in diversification rates (Appendix S2)
Finally to explore whether the temporal gap between stem and
crown ages observed in the NWTP phylogeny could be the signature
of mass extinction instead of low diversification followed by recent
radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-
dler 2011b) Following the approach by Antonelli and Sanmartın
(2011b) the shapes and the ages of Lineage Through Time (LTT)
curves of simulated trees were compared to the LTT curve observed
for the crown NWTP MCC tree Three sets of simulations were run
with the function simrateshifttaxa where only 5 of the lineages
survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-
minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)
In all sets the speciation (0223) and extinction (0180) rates were
kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200
trees were simulated to reflect stochastic variance with a final num-
ber of 54 terminals (the number of terminals in the crown NWTP
MCC tree) and accounting for the missing taxa with frac = 093
3 | RESULTS
31 | Phylogenetic analyses
The analyses of four independent loci support the sister relationship
between the tribes Cryosophileae and Sabaleae (posterior probability
[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister
in the CISP4 gene tree (Figure S21) but the alternative relationships
are not supported (PP lt 090) The comparison of individual gene
trees did not reveal other topological incongruences with PP gt095
MRBAYES and BEAST analyses of the combined partitioned dataset
recovered congruent results and the MCC tree from BEAST is shown
in Figure 2
32 | Divergence time and ancestral rangeestimation
Calibration analyses (Figure 2) inferred crown ages for the NWTP in
the Late Cretaceous (77 Ma [age values correspond to median
heights estimated with BEAST] 787ndash761 Ma [age ranges correspond
to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the
Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene
(14 Ma 187ndash96 Ma)
The most likely biogeographical model was DEC+j with dispersal
constraints (lnL = 914 Figure 3a) followed with a difference of
42 log-likelihood units by DEC with dispersal constraints
(lnL = 956) and by DEC+j without dispersal constraints
(lnL = 1024) Biogeographical analyses indicate that the NWTP
most probably originated in North America (pC = 045) sometime
during the Late Cretaceous By the Eocene Cryosophileae dispersed
to South America (pS = 067) giving rise to the genera Chelyocarpus
Itaya Sabinaria and Trithrinax Later during the early Oligocene
members of Cryosophileae dispersed back to North-Central America
and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)
Sabaleae most probably started diversifying in an area encompassing
both North America and the Caribbean islands (pNC = 050) or only
in North America (pN = 046) Two unambiguous dispersal events
from the continent to the Caribbean islands were inferred between
15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)
33 | Diversification analyses
A likelihood ratio test indicated that a model accounting for one rate
shift was strongly supported against a model without rate shifts
(mean p = 99 Table S21) Models with two or more rate shifts did
not improve model fit Figure 3b shows the mean diversification rate
as a function of time with 80 confidence interval across the 120
trees sampled A diversification rate shift was estimated around
108 Ma (SD = 80) Mean diversification rates were
0012 0014 Ma1 before the rate shift and 015 005 Ma1
after it No significant rate shifts were detected in specific branches
of the MCC tree (Figure S26) and diversification rate in Caribbean
lineages was not significantly different from that of continental
clades (Appendix S2)
Most of the trees simulated with a mass extinction occurring
66 Ma did not display the broom-and-handle shape of the empirical
tree and the crown ages of these trees were younger than the
crown NWTP age (Figure 4a median crown age 47 Ma range of
crown ages 1667ndash191 Ma) The majority of the trees simulated
under a mass extinction 35 Ma displayed the same broom-and-han-
dle shape as our empirical crown NWTP tree (Figure 4b) the crown
age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within
the lower quartile of crown ages of simulated trees which ranged
from 2039 to 218 Ma (median crown age 103 Ma) Most of the
trees simulated with a mass extinction occurring 12 Ma did not dis-
play the broom-and-handle shape of the empirical tree and their
crown ages were older than the crown NWTP age (Figure 4c med-
ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)
4 | DISCUSSION
41 | Divergence times and historical biogeography
411 | Origin of the NWTP in time and space
With all genera and 84 of species sampled our MCC tree (Fig-
ure 2) constitutes the most complete phylogenetic hypothesis
assembled to date for the NWTP Our results are congruent with
CANO ET AL | 5
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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oiorg101007s12229-008-9000-1
Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
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cal and simulated approaches Systematic Biology 60 596ndash615
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Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
National Academy of Sciences 108 8379ndash8384 httpsdoiorg10
1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
drives island radiations in the palm tribe Trachycarpeae (Arecaceae)
Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
geological models of evolution of the Isthmus of Panama in a phylo-
genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
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Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas
1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages I Historical biogeography Journal of Biogeography 40 274ndash
285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
of the Hawaiian silversword alliance (Compositae) Proceedings of the
National Academy of Sciences 95 9402ndash9406 httpsdoiorg10
1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
Chave J (2013) Origin and evolution of Chrysobalanaceae Insights
into the evolution of plants in the Neotropics Botanical Journal of the
Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339
201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-
der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
Society 151 113ndash125 httpsdoiorg101111j1095-83392006
00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
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httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
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oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
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Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
Vinent amp MacPhee 1999) and the Panama Isthmus formation start-
ing in the Miocene (Montes et al 2015) To what extent these puta-
tive corridors facilitated species dispersal across the Caribbean
region is still debated (eg Ali 2012 Nieto-Blazquez et al 2017)
and several studies postulate that overwater dispersal events have
played a major role in the biogeographical history of Caribbean plant
lineages (Cervantes et al 2016 Gugger amp Cavender-Bares 2013)
In addition to dispersal the dynamics of speciation and extinc-
tion during the history of lineages may also have influenced the cur-
rent patterns of species richness across the Caribbean and
surrounding areas (Ricklefs amp Bermingham 2008) The colonization
of archipelagos has been frequently associated with an increase of
morphological and taxonomic diversity (Bacon et al 2012 Baldwin
amp Sanderson 1998 Condamine Leslie amp Antonelli 2016 Losos amp
Ricklefs 2009) The diversification rate shift estimated for the Carib-
bean Coccothrinax (Baker amp Couvreur 2013b) the most diverse
genus of the NWTP is congruent with the hypothesis of a species
radiation triggered by island colonization Alternatively mass extinc-
tion events could also have influenced how diversity accumulated
through time (Antonelli amp Sanmartın 2011b Brocklehurst Ruta
Meurouller amp Freuroobisch 2015 Crisp amp Cook 2009) In particular three
episodes of relatively rapid climatic cooling could have affected the
diversity of frost-intolerant plants in the Caribbean region (1) the
CretaceousndashPalaeogene Event (66 Ma) when a large meteorite
impacted the Yucatan Peninsula generating immediate global dark-
ness and cooling (Schulte et al 2010) (2) the Terminal Eocene
Event (35 Ma) when global temperatures drastically dropped nega-
tively affecting the Boreotropical flora that covered large parts of
Laurasia (Morley 2003) and (3) the period following the mid-Mio-
cene climatic optimum (12 Ma) when globally warm equable cli-
mates shifted to present-day cooler and more seasonal climates
(Zachos Dickens amp Zeebe 2008) It remains unclear if the NWTP
which are considered typical elements of the Boreotropical flora
(Bjorholm Svenning Baker Skov amp Balslev 2006) were more
affected by Cenozoic cooling that caused their extirpation from Eur-
asia and northern North America (Figure 1) or by the meteorite
impact in the vicinity of their distribution range
We generated a time-calibrated species phylogeny of the NWTP
and used it to infer the biogeographical scenario that best explains
their current distribution and diversity We addressed the following
specific questions (1) When and where did the NWTP originate (2)
Is their diversity in the Caribbean the result of one or multiple dis-
persal events and which colonization routes did they follow (3)
How did island colonization and global episodes of mass extinction
influence extant NWTP diversity across the Caribbean and surround-
ing areas
2 | MATERIALS AND METHODS
21 | Taxon sampling
Our sampling includes 89 accessions from 67 species Sampling in
Cryosophileae (11 genera 35 species of 42) is complete except in
the genera Cryosophila (7 species of 10 sensu Evans 1995) and Coc-
cothrinax (10 species of 14 sensu Henderson et al 1995) Sampling
in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe-
cies of Sabal (Dransfield et al 2008) To evaluate the phylogenetic
position of the NWTP within Coryphoideae we also sampled repre-
sentatives of other tribes in this subfamily Two outgroups were
selected in subfamilies Ceroxyloideae and Arecoideae Silica-gel dried
leaf fragments were collected in the field (collection and export per-
mits 111296 and 113458 respectively from the Paraguayan Secre-
tarıa del Ambiente) or in the living collections of the Conservatoire et
Jardin botaniques de la Ville de Geneve (Switzerland) Montgomery
Botanical Center Fairchild Tropical Botanical Garden (both in the
USA) and the Jardın Botanico del Quindıo (Colombia) Voucher infor-
mation is provided in Table S11 (see Appendix S1 in Supporting
Information)
22 | Phylogenetic analyses
Four nuclear (CISP4 CISP5 PRK and RPB2) and one plastid (matK)
loci were sequenced following the protocol described in
Appendix S1 and using the primers listed in Table S12 The DNA
sequences are deposited in GenBank under the accession numbers
listed in Table S11 Sequences were aligned using MAFFT 7130
(Katoh Misawa Kuma amp Miyata 2002) Sites were scored with
GUIDANCE 141 (Penn et al 2010) and excluded from further analy-
ses if their score was lt08 to avoid adding noise to the branch
length and substitution rate estimates (Jordan amp Goldman 2012)
The final database contained 4872 bp Phylogenetic analyses were
performed on the CIPRES portal (Miller Pfeiffer amp Schwartz 2010)
Single-gene and combined partitioned phylogenetic analyses were
carried out with MRBAYES 322 (Ronquist et al 2012) In the parti-
tioned analyses the dataset was divided into five partitions corre-
sponding to each marker The best fitting substitution model for
each partition was selected from 24 models with MRAICPL 146
(Nylander 2004) using the Akaike information criterion (AIC) The
test selected the models HKY for CISP4 CISP5 and PRK GTR for
matK and GTR+Γ for RPB2 Four Markov chains were run for
5 9 106 generations with a heating temperature of 015 Samples
were logged every 100th generation Using TRACER 16 (Rambaut
Suchard Xie amp Drummond 2014) we determined burnin (24) and
confirmed trace stationarity and sufficient sampling (effective sample
size [ESS] gt200)
23 | Fossil calibration and divergence time analyses
Three fossils were used to estimate divergence times (Table S13)
Following Couvreur Forest and Baker (2011) fossils of Sabalites
carolinensis Berry and Hyphaene kappelmanii Pan et al were used to
constrain the stem nodes of subfamily Coryphoideae and subtribe
Hyphaeninae (Coryphoideae) respectively In addition fossilized
seeds of Sabal bigbendense (Manchester et al 2010) were used to
calibrate the stem node of Sabaleae These seeds from the Late Cre-
taceous (c 77 Ma) represent the oldest record attributed to the
CANO ET AL | 3
tribe Since the use of this fossil for calibrating the NWTPrsquos phy-
logeny has a strong effect on the divergence time estimates (Fig-
ure S11) a close evaluation of its relationship with the extant genus
Sabal was conducted and its classification within Sabaleae was sup-
ported (Appendix S1)
Divergence time analyses were conducted in BEAST 180 (Drum-
mond Suchard Xie amp Rambaut 2012) applying the same partitions
and substitution models as for MRBAYES Substitution and clock mod-
els were set as unlinked whereas tree models were linked among
partitions Clock model tests using stepping-stone sampling (SSS)
and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured
a relaxed clock with an uncorrelated lognormal distribution (UCLN
marginal log-likelihood = 2364194 BF = 111167) against a strict
clock (marginal log-likelihood = 2419777) We used uniform distri-
butions for UCLN mean priors for each data partition with default
initial and lower values and upper values set to 100 To assess the
impact of tree-model selection on our divergence time estimations
we compared the median node ages obtained with a Yule versus a
BirthndashDeath process model The differences ranged from 010 to
225 Ma and were markedly smaller than the 95 HPD age bars for
each model (Figure S12) indicating that both tree models yield simi-
lar divergence time estimations Because tree-model tests strongly
favoured a Yule Process (marginal log-likelihood = 2364194
BF = 7165) over a BirthndashDeath process (marginal log-
likelihood = 2367776) the Yule tree model was implemented in
further analyses
To account for uncertainty in fossil dating and identification
soft-bound lognormal priors were used for all calibration points with
standard deviations set such that 95 of the age distribution fell
within the geological time period of the fossil stratigraphic source
(Table S13 Yang amp Rannala 2006) Seven independent chains were
run for 50 9 106 generations sampling every 10000th generation
All the chains converged and their ESS values were above 200
Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-
TOR 180 (Drummond et al 2012) was used to exclude the adequate
proportion of burnin samples and obtain a maximum clade credibility
(MCC) tree displaying median heights
24 | Biogeographical analyses
Five biogeographical areas were defined (O) Old World (N) North-
Central America (S) South America (I) Panama Isthmus delimited
between the El Valle area (Panama) and the Uramita suture
(Colombia Montes et al 2015) and (C) Caribbean islands The lat-
ter were treated as a single area to facilitate understanding of bio-
tic exchanges amongst insular-continental regions A distinction
between the Greater and the Lesser Antilles was not appropriate
since most of the NWTP species occur in the Greater Antilles (34
species) and only two widespread species are present in the Lesser
Antilles Species distributions were compiled from the literature
(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans
1995 Henderson et al 1995 Zona 1990) and from the Global
Biodiversity Information Facility (GBIF httpwwwgbiforg
accessed 17 July 2014) Conflicting occurrences from GBIF (eg
palms cultivated in botanic gardens) were excluded
We inferred the biogeographical history of the NWTP using the
Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)
model (Ree amp Smith 2008) with and without the parameter ldquojrdquo
accounting for the probability of founder-event speciation as imple-
mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The
DEC+j model is appropriate in this study since the NWTP occur in
areas that have been isolated (South America the Caribbean islands)
and therefore instantaneous speciation in conjunction with long-dis-
tance dispersal may be expected Analyses were applied to the MCC
tree and tree uncertainty was considered for the interpretation of
results The tree was pruned to include a single terminal per species
The maximum number of areas at nodes was restricted to three to
simplify the computational effort and because three is the maximum
number of areas currently inhabited by any NWTP species Analyses
were conducted with and without dispersal constraints Dispersal
constraints (Table S14) were applied by assigning different dispersal
probabilities as follows p = 1 for dispersal between adjacent areas
p = 5 for dispersal over the Caribbean Sea or through non-adjacent
land areas (eg between N and S) and p = 01 for dispersal over the
Atlantic Ocean (eg between S and O) or across the fully formed
Northern Andes barrier As a sensitivity test to parameter choice
when the lowest dispersal probability was set to 01 instead of 001
no significant differences were found in the biogeographical recon-
struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141
lnL difference lt2 log-likelihood units) and relative probabilities (Fig-
ure S13)
Four time periods were defined (1) 90ndash33 Ma probability of dis-
persal from areas O to N through the Beringian and North Atlantic
land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the
Northern Hemisphere were no longer available (Brikiatis 2014) (3)
15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)
7 Ma-present final uplift of the Northern Andes acting as a barrier
for dispersal between Amazonia and Choco (Luebert amp Weiged
2014 Table S15)
25 | Diversification analyses
We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the
existence (if any) and number of diversification rate shifts in the
NWTP phylogeny A set of 120 trees were randomly chosen from
the BEAST sampling to calculate maximum likelihood estimates of spe-
ciation and extinction rates and rate shift times The function
bdshiftsoptimum was set to optimize the model parameters in 100
iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma
(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect
[Nee Holmes May amp Harvey 1994]) To determine how many rate
shifts are most probable given the phylogenies models with n and
n + 1 shifts were compared with likelihood ratio tests following the
greedy approach by Stadler (2011a) Mean and standard deviation of
diversification rates and shift ages were calculated across the 120
trees
4 | CANO ET AL
To evaluate whether shifts in diversification rate could be attrib-
uted to a specific clade we used BAMM 20 (Rabosky 2014
Appendix S2) Controversy exists regarding the adequacy of BAMM
for diversification rate inference (Moore Hohna May Rannala amp
Huelsenbeck 2016) However recent evaluations of the method
suggested that diversification rate inference with BAMM is accurate
and consistent (Rabosky Mitchell amp Chang 2017) We used the
extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-
age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether
the colonization of the Caribbean islands was associated with shifts
in diversification rates (Appendix S2)
Finally to explore whether the temporal gap between stem and
crown ages observed in the NWTP phylogeny could be the signature
of mass extinction instead of low diversification followed by recent
radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-
dler 2011b) Following the approach by Antonelli and Sanmartın
(2011b) the shapes and the ages of Lineage Through Time (LTT)
curves of simulated trees were compared to the LTT curve observed
for the crown NWTP MCC tree Three sets of simulations were run
with the function simrateshifttaxa where only 5 of the lineages
survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-
minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)
In all sets the speciation (0223) and extinction (0180) rates were
kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200
trees were simulated to reflect stochastic variance with a final num-
ber of 54 terminals (the number of terminals in the crown NWTP
MCC tree) and accounting for the missing taxa with frac = 093
3 | RESULTS
31 | Phylogenetic analyses
The analyses of four independent loci support the sister relationship
between the tribes Cryosophileae and Sabaleae (posterior probability
[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister
in the CISP4 gene tree (Figure S21) but the alternative relationships
are not supported (PP lt 090) The comparison of individual gene
trees did not reveal other topological incongruences with PP gt095
MRBAYES and BEAST analyses of the combined partitioned dataset
recovered congruent results and the MCC tree from BEAST is shown
in Figure 2
32 | Divergence time and ancestral rangeestimation
Calibration analyses (Figure 2) inferred crown ages for the NWTP in
the Late Cretaceous (77 Ma [age values correspond to median
heights estimated with BEAST] 787ndash761 Ma [age ranges correspond
to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the
Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene
(14 Ma 187ndash96 Ma)
The most likely biogeographical model was DEC+j with dispersal
constraints (lnL = 914 Figure 3a) followed with a difference of
42 log-likelihood units by DEC with dispersal constraints
(lnL = 956) and by DEC+j without dispersal constraints
(lnL = 1024) Biogeographical analyses indicate that the NWTP
most probably originated in North America (pC = 045) sometime
during the Late Cretaceous By the Eocene Cryosophileae dispersed
to South America (pS = 067) giving rise to the genera Chelyocarpus
Itaya Sabinaria and Trithrinax Later during the early Oligocene
members of Cryosophileae dispersed back to North-Central America
and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)
Sabaleae most probably started diversifying in an area encompassing
both North America and the Caribbean islands (pNC = 050) or only
in North America (pN = 046) Two unambiguous dispersal events
from the continent to the Caribbean islands were inferred between
15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)
33 | Diversification analyses
A likelihood ratio test indicated that a model accounting for one rate
shift was strongly supported against a model without rate shifts
(mean p = 99 Table S21) Models with two or more rate shifts did
not improve model fit Figure 3b shows the mean diversification rate
as a function of time with 80 confidence interval across the 120
trees sampled A diversification rate shift was estimated around
108 Ma (SD = 80) Mean diversification rates were
0012 0014 Ma1 before the rate shift and 015 005 Ma1
after it No significant rate shifts were detected in specific branches
of the MCC tree (Figure S26) and diversification rate in Caribbean
lineages was not significantly different from that of continental
clades (Appendix S2)
Most of the trees simulated with a mass extinction occurring
66 Ma did not display the broom-and-handle shape of the empirical
tree and the crown ages of these trees were younger than the
crown NWTP age (Figure 4a median crown age 47 Ma range of
crown ages 1667ndash191 Ma) The majority of the trees simulated
under a mass extinction 35 Ma displayed the same broom-and-han-
dle shape as our empirical crown NWTP tree (Figure 4b) the crown
age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within
the lower quartile of crown ages of simulated trees which ranged
from 2039 to 218 Ma (median crown age 103 Ma) Most of the
trees simulated with a mass extinction occurring 12 Ma did not dis-
play the broom-and-handle shape of the empirical tree and their
crown ages were older than the crown NWTP age (Figure 4c med-
ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)
4 | DISCUSSION
41 | Divergence times and historical biogeography
411 | Origin of the NWTP in time and space
With all genera and 84 of species sampled our MCC tree (Fig-
ure 2) constitutes the most complete phylogenetic hypothesis
assembled to date for the NWTP Our results are congruent with
CANO ET AL | 5
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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oiorg101007s12229-008-9000-1
Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-
cal and simulated approaches Systematic Biology 60 596ndash615
httpsdoiorg101093sysbiosyr062
Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
National Academy of Sciences 108 8379ndash8384 httpsdoiorg10
1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
drives island radiations in the palm tribe Trachycarpeae (Arecaceae)
Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
geological models of evolution of the Isthmus of Panama in a phylo-
genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
plex emergence of the Isthmus of Panama Proceedings of the National
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1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages I Historical biogeography Journal of Biogeography 40 274ndash
285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
of the Hawaiian silversword alliance (Compositae) Proceedings of the
National Academy of Sciences 95 9402ndash9406 httpsdoiorg10
1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
Chave J (2013) Origin and evolution of Chrysobalanaceae Insights
into the evolution of plants in the Neotropics Botanical Journal of the
Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339
201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-
der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
Society 151 113ndash125 httpsdoiorg101111j1095-83392006
00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
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iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
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httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
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Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
tribe Since the use of this fossil for calibrating the NWTPrsquos phy-
logeny has a strong effect on the divergence time estimates (Fig-
ure S11) a close evaluation of its relationship with the extant genus
Sabal was conducted and its classification within Sabaleae was sup-
ported (Appendix S1)
Divergence time analyses were conducted in BEAST 180 (Drum-
mond Suchard Xie amp Rambaut 2012) applying the same partitions
and substitution models as for MRBAYES Substitution and clock mod-
els were set as unlinked whereas tree models were linked among
partitions Clock model tests using stepping-stone sampling (SSS)
and Bayes factors (BF Kass amp Raftery 1995) very strongly favoured
a relaxed clock with an uncorrelated lognormal distribution (UCLN
marginal log-likelihood = 2364194 BF = 111167) against a strict
clock (marginal log-likelihood = 2419777) We used uniform distri-
butions for UCLN mean priors for each data partition with default
initial and lower values and upper values set to 100 To assess the
impact of tree-model selection on our divergence time estimations
we compared the median node ages obtained with a Yule versus a
BirthndashDeath process model The differences ranged from 010 to
225 Ma and were markedly smaller than the 95 HPD age bars for
each model (Figure S12) indicating that both tree models yield simi-
lar divergence time estimations Because tree-model tests strongly
favoured a Yule Process (marginal log-likelihood = 2364194
BF = 7165) over a BirthndashDeath process (marginal log-
likelihood = 2367776) the Yule tree model was implemented in
further analyses
To account for uncertainty in fossil dating and identification
soft-bound lognormal priors were used for all calibration points with
standard deviations set such that 95 of the age distribution fell
within the geological time period of the fossil stratigraphic source
(Table S13 Yang amp Rannala 2006) Seven independent chains were
run for 50 9 106 generations sampling every 10000th generation
All the chains converged and their ESS values were above 200
Trees files were combined using LOGCOMBINER 180 and TREEANNOTA-
TOR 180 (Drummond et al 2012) was used to exclude the adequate
proportion of burnin samples and obtain a maximum clade credibility
(MCC) tree displaying median heights
24 | Biogeographical analyses
Five biogeographical areas were defined (O) Old World (N) North-
Central America (S) South America (I) Panama Isthmus delimited
between the El Valle area (Panama) and the Uramita suture
(Colombia Montes et al 2015) and (C) Caribbean islands The lat-
ter were treated as a single area to facilitate understanding of bio-
tic exchanges amongst insular-continental regions A distinction
between the Greater and the Lesser Antilles was not appropriate
since most of the NWTP species occur in the Greater Antilles (34
species) and only two widespread species are present in the Lesser
Antilles Species distributions were compiled from the literature
(Bernal amp Galeano 2013 Cano Perret amp Stauffer 2013 Evans
1995 Henderson et al 1995 Zona 1990) and from the Global
Biodiversity Information Facility (GBIF httpwwwgbiforg
accessed 17 July 2014) Conflicting occurrences from GBIF (eg
palms cultivated in botanic gardens) were excluded
We inferred the biogeographical history of the NWTP using the
Maximum Likelihood-based DispersalndashExtinctionndashCladogenesis (DEC)
model (Ree amp Smith 2008) with and without the parameter ldquojrdquo
accounting for the probability of founder-event speciation as imple-
mented in the R package ldquoBioGeoBEARSrdquo (Matzke 2014) The
DEC+j model is appropriate in this study since the NWTP occur in
areas that have been isolated (South America the Caribbean islands)
and therefore instantaneous speciation in conjunction with long-dis-
tance dispersal may be expected Analyses were applied to the MCC
tree and tree uncertainty was considered for the interpretation of
results The tree was pruned to include a single terminal per species
The maximum number of areas at nodes was restricted to three to
simplify the computational effort and because three is the maximum
number of areas currently inhabited by any NWTP species Analyses
were conducted with and without dispersal constraints Dispersal
constraints (Table S14) were applied by assigning different dispersal
probabilities as follows p = 1 for dispersal between adjacent areas
p = 5 for dispersal over the Caribbean Sea or through non-adjacent
land areas (eg between N and S) and p = 01 for dispersal over the
Atlantic Ocean (eg between S and O) or across the fully formed
Northern Andes barrier As a sensitivity test to parameter choice
when the lowest dispersal probability was set to 01 instead of 001
no significant differences were found in the biogeographical recon-
struction in terms of likelihood (lnL01 = 9335 lnL001 = 9141
lnL difference lt2 log-likelihood units) and relative probabilities (Fig-
ure S13)
Four time periods were defined (1) 90ndash33 Ma probability of dis-
persal from areas O to N through the Beringian and North Atlantic
land bridges (Brikiatis 2014) (2) 33ndash15 Ma land bridges in the
Northern Hemisphere were no longer available (Brikiatis 2014) (3)
15ndash7 Ma Panama Isthmus closure (Montes et al 2015) and (4)
7 Ma-present final uplift of the Northern Andes acting as a barrier
for dispersal between Amazonia and Choco (Luebert amp Weiged
2014 Table S15)
25 | Diversification analyses
We used the R package ldquoTreeParrdquo (Stadler 2011a) to detect the
existence (if any) and number of diversification rate shifts in the
NWTP phylogeny A set of 120 trees were randomly chosen from
the BEAST sampling to calculate maximum likelihood estimates of spe-
ciation and extinction rates and rate shift times The function
bdshiftsoptimum was set to optimize the model parameters in 100
iterations (maxitk) every 1 Myr (grid) from 90 Ma (end) to 5 Ma
(start and not to 0 Ma to avoid the ldquopull of the presentrdquo effect
[Nee Holmes May amp Harvey 1994]) To determine how many rate
shifts are most probable given the phylogenies models with n and
n + 1 shifts were compared with likelihood ratio tests following the
greedy approach by Stadler (2011a) Mean and standard deviation of
diversification rates and shift ages were calculated across the 120
trees
4 | CANO ET AL
To evaluate whether shifts in diversification rate could be attrib-
uted to a specific clade we used BAMM 20 (Rabosky 2014
Appendix S2) Controversy exists regarding the adequacy of BAMM
for diversification rate inference (Moore Hohna May Rannala amp
Huelsenbeck 2016) However recent evaluations of the method
suggested that diversification rate inference with BAMM is accurate
and consistent (Rabosky Mitchell amp Chang 2017) We used the
extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-
age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether
the colonization of the Caribbean islands was associated with shifts
in diversification rates (Appendix S2)
Finally to explore whether the temporal gap between stem and
crown ages observed in the NWTP phylogeny could be the signature
of mass extinction instead of low diversification followed by recent
radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-
dler 2011b) Following the approach by Antonelli and Sanmartın
(2011b) the shapes and the ages of Lineage Through Time (LTT)
curves of simulated trees were compared to the LTT curve observed
for the crown NWTP MCC tree Three sets of simulations were run
with the function simrateshifttaxa where only 5 of the lineages
survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-
minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)
In all sets the speciation (0223) and extinction (0180) rates were
kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200
trees were simulated to reflect stochastic variance with a final num-
ber of 54 terminals (the number of terminals in the crown NWTP
MCC tree) and accounting for the missing taxa with frac = 093
3 | RESULTS
31 | Phylogenetic analyses
The analyses of four independent loci support the sister relationship
between the tribes Cryosophileae and Sabaleae (posterior probability
[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister
in the CISP4 gene tree (Figure S21) but the alternative relationships
are not supported (PP lt 090) The comparison of individual gene
trees did not reveal other topological incongruences with PP gt095
MRBAYES and BEAST analyses of the combined partitioned dataset
recovered congruent results and the MCC tree from BEAST is shown
in Figure 2
32 | Divergence time and ancestral rangeestimation
Calibration analyses (Figure 2) inferred crown ages for the NWTP in
the Late Cretaceous (77 Ma [age values correspond to median
heights estimated with BEAST] 787ndash761 Ma [age ranges correspond
to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the
Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene
(14 Ma 187ndash96 Ma)
The most likely biogeographical model was DEC+j with dispersal
constraints (lnL = 914 Figure 3a) followed with a difference of
42 log-likelihood units by DEC with dispersal constraints
(lnL = 956) and by DEC+j without dispersal constraints
(lnL = 1024) Biogeographical analyses indicate that the NWTP
most probably originated in North America (pC = 045) sometime
during the Late Cretaceous By the Eocene Cryosophileae dispersed
to South America (pS = 067) giving rise to the genera Chelyocarpus
Itaya Sabinaria and Trithrinax Later during the early Oligocene
members of Cryosophileae dispersed back to North-Central America
and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)
Sabaleae most probably started diversifying in an area encompassing
both North America and the Caribbean islands (pNC = 050) or only
in North America (pN = 046) Two unambiguous dispersal events
from the continent to the Caribbean islands were inferred between
15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)
33 | Diversification analyses
A likelihood ratio test indicated that a model accounting for one rate
shift was strongly supported against a model without rate shifts
(mean p = 99 Table S21) Models with two or more rate shifts did
not improve model fit Figure 3b shows the mean diversification rate
as a function of time with 80 confidence interval across the 120
trees sampled A diversification rate shift was estimated around
108 Ma (SD = 80) Mean diversification rates were
0012 0014 Ma1 before the rate shift and 015 005 Ma1
after it No significant rate shifts were detected in specific branches
of the MCC tree (Figure S26) and diversification rate in Caribbean
lineages was not significantly different from that of continental
clades (Appendix S2)
Most of the trees simulated with a mass extinction occurring
66 Ma did not display the broom-and-handle shape of the empirical
tree and the crown ages of these trees were younger than the
crown NWTP age (Figure 4a median crown age 47 Ma range of
crown ages 1667ndash191 Ma) The majority of the trees simulated
under a mass extinction 35 Ma displayed the same broom-and-han-
dle shape as our empirical crown NWTP tree (Figure 4b) the crown
age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within
the lower quartile of crown ages of simulated trees which ranged
from 2039 to 218 Ma (median crown age 103 Ma) Most of the
trees simulated with a mass extinction occurring 12 Ma did not dis-
play the broom-and-handle shape of the empirical tree and their
crown ages were older than the crown NWTP age (Figure 4c med-
ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)
4 | DISCUSSION
41 | Divergence times and historical biogeography
411 | Origin of the NWTP in time and space
With all genera and 84 of species sampled our MCC tree (Fig-
ure 2) constitutes the most complete phylogenetic hypothesis
assembled to date for the NWTP Our results are congruent with
CANO ET AL | 5
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
REFERENCES
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Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
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cal and simulated approaches Systematic Biology 60 596ndash615
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Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
National Academy of Sciences 108 8379ndash8384 httpsdoiorg10
1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
drives island radiations in the palm tribe Trachycarpeae (Arecaceae)
Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
geological models of evolution of the Isthmus of Panama in a phylo-
genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
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Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas
1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
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285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
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1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
Chave J (2013) Origin and evolution of Chrysobalanaceae Insights
into the evolution of plants in the Neotropics Botanical Journal of the
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201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-
der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
Society 151 113ndash125 httpsdoiorg101111j1095-83392006
00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
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of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
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1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
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Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
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graphic range evolution by dispersal local extinction and cladogene-
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10635150701883881
CANO ET AL | 11
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biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
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of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
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Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
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tree201105011
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Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
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Stadler T (2011a) Mammalian phylogeny reveals recent diversification
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cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
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Miocene of France) Anatomy palaeobiogeography and evolutionary
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Molecular phylogenetics and biogeography of the Caribbean-centered
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times under a molecular clock using multiple fossil calibrations with
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oiorg101093molbevmsj024
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perspective on greenhouse warming and carbon-cycle dynamics Nat-
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Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
To evaluate whether shifts in diversification rate could be attrib-
uted to a specific clade we used BAMM 20 (Rabosky 2014
Appendix S2) Controversy exists regarding the adequacy of BAMM
for diversification rate inference (Moore Hohna May Rannala amp
Huelsenbeck 2016) However recent evaluations of the method
suggested that diversification rate inference with BAMM is accurate
and consistent (Rabosky Mitchell amp Chang 2017) We used the
extension GeoSSE (Goldberg Lancaster amp Ree 2011) of the R pack-
age ldquoDiversitreerdquo (FitzJohn Maddison amp Otto 2009) to test whether
the colonization of the Caribbean islands was associated with shifts
in diversification rates (Appendix S2)
Finally to explore whether the temporal gap between stem and
crown ages observed in the NWTP phylogeny could be the signature
of mass extinction instead of low diversification followed by recent
radiation trees were simulated with the R package ldquoTreeSimrdquo (Sta-
dler 2011b) Following the approach by Antonelli and Sanmartın
(2011b) the shapes and the ages of Lineage Through Time (LTT)
curves of simulated trees were compared to the LTT curve observed
for the crown NWTP MCC tree Three sets of simulations were run
with the function simrateshifttaxa where only 5 of the lineages
survived (1) the CretaceousndashPalaeogene Event (66 Ma) (2) the Ter-
minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma)
In all sets the speciation (0223) and extinction (0180) rates were
kept constant (values extracted from ldquoTreeParrdquo for 0 shifts) and 200
trees were simulated to reflect stochastic variance with a final num-
ber of 54 terminals (the number of terminals in the crown NWTP
MCC tree) and accounting for the missing taxa with frac = 093
3 | RESULTS
31 | Phylogenetic analyses
The analyses of four independent loci support the sister relationship
between the tribes Cryosophileae and Sabaleae (posterior probability
[PP] gt090 see Figures S22ndash5 in Appendix S2) They are not sister
in the CISP4 gene tree (Figure S21) but the alternative relationships
are not supported (PP lt 090) The comparison of individual gene
trees did not reveal other topological incongruences with PP gt095
MRBAYES and BEAST analyses of the combined partitioned dataset
recovered congruent results and the MCC tree from BEAST is shown
in Figure 2
32 | Divergence time and ancestral rangeestimation
Calibration analyses (Figure 2) inferred crown ages for the NWTP in
the Late Cretaceous (77 Ma [age values correspond to median
heights estimated with BEAST] 787ndash761 Ma [age ranges correspond
to 95 HPD ranges estimated with BEAST]) for Cryosophileae in the
Eocene (45 Ma 562ndash346 Ma) and for Sabaleae in the Miocene
(14 Ma 187ndash96 Ma)
The most likely biogeographical model was DEC+j with dispersal
constraints (lnL = 914 Figure 3a) followed with a difference of
42 log-likelihood units by DEC with dispersal constraints
(lnL = 956) and by DEC+j without dispersal constraints
(lnL = 1024) Biogeographical analyses indicate that the NWTP
most probably originated in North America (pC = 045) sometime
during the Late Cretaceous By the Eocene Cryosophileae dispersed
to South America (pS = 067) giving rise to the genera Chelyocarpus
Itaya Sabinaria and Trithrinax Later during the early Oligocene
members of Cryosophileae dispersed back to North-Central America
and colonized the Caribbean islands (around 28 Ma 341ndash213 Ma)
Sabaleae most probably started diversifying in an area encompassing
both North America and the Caribbean islands (pNC = 050) or only
in North America (pN = 046) Two unambiguous dispersal events
from the continent to the Caribbean islands were inferred between
15ndash4 Ma (97 Ma) and between 6ndash2 Ma (37 Ma)
33 | Diversification analyses
A likelihood ratio test indicated that a model accounting for one rate
shift was strongly supported against a model without rate shifts
(mean p = 99 Table S21) Models with two or more rate shifts did
not improve model fit Figure 3b shows the mean diversification rate
as a function of time with 80 confidence interval across the 120
trees sampled A diversification rate shift was estimated around
108 Ma (SD = 80) Mean diversification rates were
0012 0014 Ma1 before the rate shift and 015 005 Ma1
after it No significant rate shifts were detected in specific branches
of the MCC tree (Figure S26) and diversification rate in Caribbean
lineages was not significantly different from that of continental
clades (Appendix S2)
Most of the trees simulated with a mass extinction occurring
66 Ma did not display the broom-and-handle shape of the empirical
tree and the crown ages of these trees were younger than the
crown NWTP age (Figure 4a median crown age 47 Ma range of
crown ages 1667ndash191 Ma) The majority of the trees simulated
under a mass extinction 35 Ma displayed the same broom-and-han-
dle shape as our empirical crown NWTP tree (Figure 4b) the crown
age of our empirical NWTP tree (77 Ma 787ndash761 Ma) fell within
the lower quartile of crown ages of simulated trees which ranged
from 2039 to 218 Ma (median crown age 103 Ma) Most of the
trees simulated with a mass extinction occurring 12 Ma did not dis-
play the broom-and-handle shape of the empirical tree and their
crown ages were older than the crown NWTP age (Figure 4c med-
ian crown age = 115 Ma range of crown ages 1872ndash741 Ma)
4 | DISCUSSION
41 | Divergence times and historical biogeography
411 | Origin of the NWTP in time and space
With all genera and 84 of species sampled our MCC tree (Fig-
ure 2) constitutes the most complete phylogenetic hypothesis
assembled to date for the NWTP Our results are congruent with
CANO ET AL | 5
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
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cal and simulated approaches Systematic Biology 60 596ndash615
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Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
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1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
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syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
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Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
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1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
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285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
of the Hawaiian silversword alliance (Compositae) Proceedings of the
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1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
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into the evolution of plants in the Neotropics Botanical Journal of the
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201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
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21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
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00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
F IGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST All posterior probabilities were above090 unless otherwise indicated Bars indicate 95 highest posterior densities of ages The three fossils used for calibration are (1) Sabalitescarolinensis (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset fossil seed modified from Manchester et al [2010] bar scale 5 mm) areindicated with their placement on the tree Trithrinax campestris from Cordoba (Argentina) is shown (bottom left credit Angela Cano)
6 | CANO ET AL
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
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Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
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Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
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Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
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Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
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Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
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Baker W J amp Couvreur T L P (2013b) Global biogeography and
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Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
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into the evolution of plants in the Neotropics Botanical Journal of the
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Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
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21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
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Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
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Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
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Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
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Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
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Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
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impact of the branching process prior in Bayesian molecular dating
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015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
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sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
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Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
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rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
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ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
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1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
F IGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae (a) Ancestral ranges estimated using the DispersalndashExtinctionndashCladogenesis +j model Pie charts represent the relative probabilities of ancestral areas where white represents 4th to last probablestates combined Inset biogeographical regions (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excludedto avoid the ldquopull of the presentrdquo effect [Nee et al 1994]) where the black curve is the mean diversification rate estimated from 120 treesthe grey area is the 80 confidence interval and a rate shift at 108 Ma detected with the ldquoTreeParrdquo analysis is marked by a dashed line
CANO ET AL | 7
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
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Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
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Baker W J amp Couvreur T L P (2013b) Global biogeography and
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Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
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Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
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World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
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Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
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Cano A Perret M amp Stauffer F W (2013) A revision of the genus
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Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
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Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
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Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
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015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
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Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
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sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
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Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
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Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
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Origin and diversification of hutias unravelled by next-generation
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Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
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ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
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Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
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1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
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20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
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1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
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Molecular phylogenetics and biogeography of the Caribbean-centered
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Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
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oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
previous molecular phylogenetic studies and morphological studies
(see Appendix S3 for further discussion) However divergence time
analyses (Figure 2) inferred much older node ages for the stem and
crown of the NWTP (median ages 82 and 77 Ma respectively) and
for the crown of Cryosophileae (45 Ma) than previously estimated
(eg Couvreur et al 2011 Faurby Eiserhardt Baker amp Svenning
2016 Figure S27) The use of different taxonomic sampling dating
methods or calibration points could explain those differences Here
however the most likely explanation is our use of the fossil Sabal
bigbendense (Manchester et al 2010) which strongly influenced esti-
mates of divergence times (Figure S11) and which has not previ-
ously been considered in divergence-time analyses of palms We do
not think we placed the fossil calibration incorrectly because our
reassessment of its affinities (Appendix S1) confirmed Manchester
et alrsquos (2010) placement of it in Sabal We predict that the calibrated
molecular dating palm genera by Couvreur et al (2011) would have
estimated older node ages for the NWTP if they had used the fossil
S bigbendense as a node constraint The downstream consequences
of this are minor for the NWTP diversification studies since its bio-
geographical history is here explored for the first time in detail
However further evaluation of S bigbendense as a calibration point
is necessary to assess the biogeography of palms at the global scale
Our biogeographical estimation indicates that the most recent
common ancestor of the NWTP was most probably distributed in
Laurasia (Figure 3a PN = 045) but other geographical origins for
the NWTP were also recovered although with lower relative proba-
bilities (Figure 3a PS = 023 PNS = 014) A Laurasian origin agrees
with the scenario posed by Baker and Couvreur (2013a) in which
the origin of the NWTP was inferred to be North America It is
also consistent with fossils of Sabal and Cryosophileae occurring in
a wide range of localities in the Northern Hemisphere including
Europe since the Early Eocene for Sabal and Early Oligocene for
Cryosophileae (Figure 1 Manchester et al 2010 Thomas amp De
Franceschi 2012) Taken together these elements indicate that
ancestors of the NWTP were probably a component of the
Boreotropical plant assemblage that covered most of the southern
part of North America and Eurasia during the Palaeocene and early
Eocene (Bjorholm et al 2006)
Our most probable scenario hypothesizes that from North
America Cryosophileae colonized South America where they began
to diversify around 45 Ma (562ndash346 Ma) This dispersal likely
occurred overwater or via stepping stones along the Proto-Antilles
that may have facilitated the Eocene colonization of South America
as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma
Cuenca et al 2008) and other plant groups including Chrysobal-
anaceae (47 Ma Bardon et al 2013) Cinchonoideae (Rubiaceae
492 Ma Antonelli Nylander Persson amp Sanmartın 2009) and Helio-
tropium (Heliotropiaceae 457 Ma Luebert Hilger amp Weigend
2011) among others Diversification of Cryosophileae gave rise to
lineages that today occur in subtropical South America (Trithrinax)
and in Western Amazonia (Chelyocarpus and Itaya) Such distribu-
tions deep inland in the tropical rain forest are quite distinct from
those of other Cryosophileae which occur closer to the coast How-
ever during the Miocene a marine incursion prolonged by the
Palaeo-Orinoco fluvial system periodically connected the Western
Amazonian drainage to the Caribbean coast (Hoorn et al 2010 Jar-
amillo et al 2017 Salamanca Villegas et al 2016) We postulate
that this marine incursion and its wetland extensions could have
provided corridors facilitating the propagation of these palms deep
inside South America
412 | Multiple dispersal events to the Caribbeanislands
Our biogeographical reconstruction inferred four dispersal events
from the mainland to the Caribbean islands The most probable sce-
nario had Cryosophileae first dispersing from South America into
North-Central America around 31 Ma (389ndash249 Ma) then into the
Caribbean islands around 28 Ma (341ndash213 Ma Figure 3a) Such
dispersal could have happened overwater as has been inferred for
various groups of animals (eg Fabre et al 2014) and plants (Cer-
vantes et al 2016) Although less likely our reconstruction also
attributed a probability (pNC = 017 pC = 016) to the hypothesis
that the Cryosophileae first colonized the Caribbean islands from
South America during the early Oligocene (Figure 3a) This alterna-
tive dispersal route coincides with the hypothesized GAARlandia
F IGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey)simulated under mass extinction conditions (5 lineage survival) (a) CretaceousndashPalaeogene Event (66 Ma) (b) Terminal Eocene Event (35 Ma)(c) Mid-Miocene Event with speciation (0223) and extinction (0180) rates extracted from the ldquoTreeParrdquo analysis of 0 shifts Boxplotssummarize the simulated treesrsquo crown ages the median is indicated by a vertical line that divides the 25th and 75th percentiles of the dataand the whiskers show the maximum and minimum values excluding outliers
8 | CANO ET AL
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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Baker W J amp Couvreur T L P (2013b) Global biogeography and
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Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
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Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
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00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
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geography 41 1036ndash1054 httpsdoiorg101111jbi12310
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Cano A Perret M amp Stauffer F W (2013) A revision of the genus
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Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
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Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
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Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
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015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
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1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
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Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
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sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
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Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
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rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
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ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
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1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
corridor (Iturralde-Vinent amp MacPhee 1999) that might have existed
around the same time although evidence supporting the existence
of this corridor is not conclusive (Ali 2012 Nieto-Blazquez et al
2017)
Our results also identify more recent island-mainland exchanges
(Figure 3) Dispersal from North-Central America into the Caribbean
islands during the Pliocene probably gave rise to the Caribbean
endemic clade of Sabal causiarum S domingensis and S maritima
During the same period dispersal events in the opposite direction
were also inferred in Cryosophileae explaining the extant distribution
of Coccothrinax argentata and Thrinax radiata in North-Central Amer-
ica These frequent overwater dispersal events reconstructed for the
NWTP corroborate Baker and Couvreurrsquos (2013a) observation that
long-distance dispersal is a key mechanism underpinning the distri-
bution of palm lineages
42 | Diversification of the NWTP radiation in theCaribbean or mass extinction
We did not find evidence that the diversification rate of the NWTP
in the Caribbean was higher than in continental areas (Appendix S2)
but there was a rate shift across the group as a whole between 137
and 62 Ma (108 Ma Figure 3) Although diversification in Coc-
cothrinax Cryosophila and Sabal increased around that time rate
shifts were not significant in any of these specific lineages (Fig-
ure S26) contradicting a previous diversification analysis that
reported a significant rate shift at the stem node of Coccothrinax
(Baker amp Couvreur 2013b) The difference might be explained by
sampling the latter included only one representative of each genus
with diversification rate derived from species counts whereas we
used a species-level phylogeny but with four of the 14 species
excluded because of missing data Also the rate shift detected by
our ldquoTreeParrdquo analyses occurred about 17 Myr after the recon-
structed dispersal of Cryosophileae into the islands rather than con-
temporaneous with colonization Therefore a causal link between
island colonization and increased diversification is rejected for the
NWTP Instead the diversification rate increase coincides temporally
with the mid-Miocene cooling that enhanced the expansion of arid
and semi-arid environments in tropical America (Graham 2010)
Since the greatest diversity of the NTWP is found in dry environ-
ments outside the tropical rain forest (eg Coccothrinax and Sabal)
we hypothesize that the shift to increased seasonality during the
mid-Miocene could have triggered an increase in diversification rate
for the NWTP as in other plant groups such as Cactaceae and
cycads (Arakaki et al 2011 Condamine Nagalingum Marshall amp
Morlon 2015)
The wider geographical distribution of the NWTP in the past
than today (Figure 1) and the two particularly long branches (at least
20 and 57 Myr) leading to the crown nodes of Cryosophileae and
Sabaleae (Figure 2) suggest that extinctions could also have
impacted the diversification of these tribes Indeed tree simulations
have demonstrated that broom-and-handle patterns can result from
ancient mass extinction (Antonelli amp Sanmartın 2011b Crisp amp
Cook 2009) and our simulations indicate that this hypothesis can-
not be rejected for the NWTP The shapes and ages of LTT plots of
trees simulated under a mass extinction at the Terminal Eocene
Event (35 Ma) match most closely those of the NWTP (Figure 4b)
Contrastingly simulations of a mass extinction at the Cretaceousndash
Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma) did
not show the same pattern crown ages from these simulated mass
extinctions are either too young or too old and show a less evident
broom-and-handle shape (Figure 4ac) These results suggest that the
diversification pattern reconstructed for the NWTP could be related
to a mass extinction event at the Terminal Eocene and a later re-
diversification of the surviving lineages at lower latitudes since the
mid-Miocene The colder conditions at the end of the Eocene could
explain why these elements of the Boreotropical flora were extir-
pated from the northern latitudes (Figure 1 Bjorholm et al 2006)
and may reflect events in other evergreen frost-intolerant taxa that
were once part of the Boreotropical flora but became extinct or
migrated southwards (Jaramillo Rueda amp Mora 2006 Morley
2003) Nevertheless we have not excluded the possibility that a Ter-
minal Eocene extinction event overwrote the signature of an earlier
extinction (eg CretaceousndashPalaeogene) from the diversification pat-
terns recovered for the NWTP
5 | CONCLUSIONS
We identified two main biogeographical explanations for the distri-
bution of the NWTP in the Caribbean region and surrounding land-
masses First a pre-Panama Isthmus colonization of South America
from Laurasia during the Eocene following a dispersal route shared
by other Boreotropical plants (eg Antonelli et al 2009 Bardon
et al 2013 Cuenca et al 2008 Luebert et al 2011) Second a
recolonization of North-Central America around 31 Ma (389ndash
249 Ma) and a subsequent dispersal to the Caribbean islands around
28 Ma (341ndash213) which most probably occurred overwater rather
than through GAARlandia Later overwater dispersal events appear
to have contributed little to the Caribbean species richness of the
NWTP which mainly underwent local diversification We did not
find that island lineages diversified at a higher rate than those on
continents Instead we suggest that the diversification history of
these palms with a long temporal gap from their origin to the begin-
ning of their diversification could reflect the signature of mass
extinction The global climatic cooling at the end of the Eocene
might have had a more significant impact on the diversity and distri-
bution of Caribbean plants
ACKNOWLEDGEMENTS
AC was supported by the International Palm Society Endowment
Fund the Augustin Lombard grant the Commission of the travel
grant and the Foundation Dr Joachim de Giacomi of the Academie
des sciences naturelles Suisse the International Association for Plant
Taxonomy and the Fondation Schmidheiny MP was funded by the
CANO ET AL | 9
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
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Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
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cal and simulated approaches Systematic Biology 60 596ndash615
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Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
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Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
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Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
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genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
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Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas
1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
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285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
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Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
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1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
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into the evolution of plants in the Neotropics Botanical Journal of the
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201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
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der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
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00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
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Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
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101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
Swiss National Science Foundation (31003A_1756551) CDB and
AA were funded by the Swedish (B0569601) and European
(331024 FP2007-2013) Research Councils a Wallenberg Academy
Fellowship and the Swedish Foundation for Strategic Research We
thank R Bernal G Galeanodagger HF Manrique (JBQ) M Gonzalez S
Da-Giau P Griffith and L Noblick (MBC) CE Lewis C Husby and
M Griffiths (FTBG) and R Niba for facilitating samples and data col-
lection and I Sanmartın for her guidance in the simulation analyses
We thank MN Dawson L Cook and J Roncal for their valuable
insights into the manuscript
ORCID
Angela Cano httporcidorg0000-0002-5090-7730
Christine D Bacon httporcidorg0000-0003-2341-2705
REFERENCES
Acevedo-Rodrıguez P amp Strong M T (2008) Floristic richness and
affinities in the West Indies The Botanical Review 74 5ndash36 httpsd
oiorg101007s12229-008-9000-1
Ali J R (2012) Colonizing the Caribbean Is the GAARlandia land-bridge
hypothesis gaining a foothold Commentary Journal of Biogeography
39 431ndash433 httpsdoiorg101111j1365-2699201102674x
Antonelli A Nylander J A Persson C amp Sanmartın I (2009) Tracingthe impact of the Andean uplift on Neotropical plant evolution Pro-
ceedings of the National Academy of Sciences 106 9749ndash9754
httpsdoiorg101073pnas0811421106
Antonelli A amp Sanmartın I (2011a) Why are there so many plant spe-
cies in the Neotropics Taxon 60 403ndash414
Antonelli A amp Sanmartın I (2011b) Mass extinction gradual cooling or
rapid radiation Reconstructing the spatiotemporal evolution of the
ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri-
cal and simulated approaches Systematic Biology 60 596ndash615
httpsdoiorg101093sysbiosyr062
Arakaki M Christin P-A Nyffeler R Lendel A Eggli U Ogburn R
M Edwards E J (2011) Contemporaneous and recent radiations
of the worldrsquos major succulent plant lineages Proceedings of the
National Academy of Sciences 108 8379ndash8384 httpsdoiorg10
1073pnas1100628108
Bacon C D Baker W J amp Simmons M P (2012) Miocene dispersal
drives island radiations in the palm tribe Trachycarpeae (Arecaceae)
Systematic Biology 61 426ndash442 httpsdoiorg101093sysbio
syr123
Bacon C D Mora A Wagner W L amp Jaramillo C A (2013) Testing
geological models of evolution of the Isthmus of Panama in a phylo-
genetic framework Botanical Journal of the Linnean Society 171
287ndash300 httpsdoiorg101111j1095-8339201201281x
Bacon C D Silvestro D Jaramillo C Smith B T Chakrabarty P amp
Antonelli A (2015) Biological evidence supports an early and com-
plex emergence of the Isthmus of Panama Proceedings of the National
Academy of Sciences 112 6110ndash6115 httpsdoiorg101073pnas
1423853112
Baker W J amp Couvreur T L P (2013a) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages I Historical biogeography Journal of Biogeography 40 274ndash
285
Baker W J amp Couvreur T L P (2013b) Global biogeography and
diversification of palms sheds light on the evolution of tropical lin-
eages II Diversification history and origin of regional assemblages
Journal of Biogeography 40 286ndash298 httpsdoiorg101111j
1365-2699201202794x
Baldwin B G amp Sanderson M J (1998) Age and rate of diversification
of the Hawaiian silversword alliance (Compositae) Proceedings of the
National Academy of Sciences 95 9402ndash9406 httpsdoiorg10
1073pnas95169402
Bardon L Chamagne J Dexter K G Sothers C A Prance G T amp
Chave J (2013) Origin and evolution of Chrysobalanaceae Insights
into the evolution of plants in the Neotropics Botanical Journal of the
Linnean Society 171 19ndash37 httpsdoiorg101111j1095-8339
201201289x
Bernal R amp Galeano G (2013) Sabinaria a new genus of palms (Cryo-
sophileae Coryphoideae Arecaceae) from the Colombia-Panama bor-
der Phytotaxa 144 27ndash44 httpsdoiorg1011646phytotaxa144
21
Bjorholm S Svenning J-C Baker W J Skov F amp Balslev H (2006)
Historical legacies in the geographical diversity patterns of New
World palm (Arecaceae) subfamilies Botanical Journal of the Linnean
Society 151 113ndash125 httpsdoiorg101111j1095-83392006
00527x
Brikiatis L (2014) The De Geer Thulean and Beringia routes Key con-
cepts for understanding early Cenozoic biogeography Journal of Bio-
geography 41 1036ndash1054 httpsdoiorg101111jbi12310
Brocklehurst N Ruta M Meurouller J amp Freuroobisch J (2015) Elevated
extinction rates as a trigger for diversification rate shifts Early
amniotes as a case study Scientific Reports 5 17104 httpsdoiorg
101038srep17104
Cano A Perret M amp Stauffer F W (2013) A revision of the genus
Trithrinax (Cryosophileae Coryphoideae Arecaceae) Phytotaxa 136
1ndash53
Cervantes A Fuentes S Gutierrez J Magallon S amp Borsch T (2016)
Successive arrivals since the Miocene shaped the diversity of the
Caribbean Acalyphoideae (Euphorbiaceae) Journal of Biogeography
43 1773ndash1785 httpsdoiorg101111jbi12790
Condamine F L Leslie A B amp Antonelli A (2016) Ancient islands
acted as refugia and pumps for conifer diversity Cladistics 33 69ndash
92
Condamine F L Nagalingum N S Marshall C R amp Morlon H (2015)
Origin and diversification of living cycads A cautionary tale on the
impact of the branching process prior in Bayesian molecular dating
BMC Evolutionary Biology 15 65 httpsdoiorg101186s12862-
015-0347-8
Couvreur T L Forest F amp Baker W J (2011) Origin and global diver-
sification patterns of tropical rain forests Inferences from a complete
genus-level phylogeny of palms BMC Biology 9 44 httpsdoiorg
1011861741-7007-9-44
Crisp M D amp Cook L G (2009) Explosive radiation or cryptic mass
extinction Interpreting signatures in molecular phylogenies Evolution
63 2257ndash2265 httpsdoiorg101111j1558-5646200900728x
Cuenca A Asmussen-Lange C B amp Borchsenius F (2008) A dated
phylogeny of the palm tribe Chamaedoreeae supports Eocene disper-
sal between Africa North and South America Molecular Phylogenetics
and Evolution 46 760ndash775 httpsdoiorg101016jympev2007
10010
Dransfield J B Uhl N W Asmussen C B Baker W J Harley M M
amp Lewis C E (2008) Genera Palmarum - The evolution and classifica-
tion of palms Richmond UK Kew Publishing
Drummond A J Suchard M A Xie D amp Rambaut A (2012) Bayesian
phylogenetics with BEAUti and the BEAST 17 Molecular Biology and
Evolution 29 1969ndash1973 httpsdoiorg101093molbevmss075
Evans R J (1995) Systematics of Cryosophila (Palmae) Systematic Bot-
any Monographs 46 1ndash70 httpsdoiorg10230725027854
Fabre P-H Vilstrup J T Raghavan M Sarkissian C D Willerslev E
Douzery E J P amp Orlando L (2014) Rodents of the Caribbean
Origin and diversification of hutias unravelled by next-generation
10 | CANO ET AL
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
museomics Biology Letters 10 20140266 httpsdoiorg101098
rsbl20140266
Faurby S Eiserhardt W L Baker W J amp Svenning J-C (2016) An
all-evidence species-level supertree for the palms (Arecaceae) Molec-
ular Phylogenetics and Evolution 100 57ndash69 httpsdoiorg10
1016jympev201603002
Filipowicz N amp Renner S S (2012) Brunfelsia (Solanaceae) A genus
evenly divided between South America and radiations on Cuba and
other Antillean islands Molecular Phylogenetics and Evolution 64 1ndash
11 httpsdoiorg101016jympev201202026
FitzJohn R G Maddison W P amp Otto S P (2009) Estimating trait-
dependent speciation and extinction rates from incompletely resolved
phylogenies Systematic Biology 58 595ndash611 httpsdoiorg10
1093sysbiosyp067
Francisco-Ortega J Santiago-Valentın E Acevedo-Rodrıguez P Lewis
C Pipoly J Meerow A W amp Maunder M (2007) Seed plant gen-
era endemic to the Caribbean Island biodiversity hotspot A review
and a molecular phylogenetic perspective The Botanical Review 73
183ndash234 httpsdoiorg1016630006-8101(2007)73[183SPGETT]
20CO2
Goldberg E E Lancaster L T amp Ree R H (2011) Phylogenetic infer-
ence of reciprocal effects between geographic range evolution and
diversification Systematic Biology 60 451ndash465 httpsdoiorg10
1093sysbiosyr046
Graham A (2003) Historical phytogeography of the Greater Antilles
Brittonia 55 357ndash383 httpsdoiorg1016630007-196X(2003)
055[0357HPOTGA]20CO2
Graham A (2010) Late Cretaceous and Cenozoic History of Latin American
Vegetation and Terrestrial Environments St Louis MO Missouri
Botanical Garden Press
Gugger P F amp Cavender-Bares J (2013) Molecular and morphologi-
cal support for a Florida origin of the Cuban oak Journal of Bio-
geography 40 632ndash645 httpsdoiorg101111j1365-26992011
02610x
Henderson A Galeano G amp Bernal R (1995) Field guide to the palms
of the Americas Princeton NJ USA Princeton University Press
Hoorn C Wesselingh F P ter Steege H Bermudez M A Mora A amp
Sevink J Antonelli A (2010) Amazonia through time Andean
uplift climate change landscape evolution and biodiversity Science
330 927ndash931 httpsdoiorg101126science1194585
Iturralde-Vinent M amp MacPhee R D (1999) Paleogeography of the
Caribbean region Implications for Cenozoic biogeography Bulletin of
the American Museum of Natural History 238 1ndash95
Jaramillo C Romero I DrsquoApolito C Bayona G Duarte E Louwye S
Wesselingh F P (2017) Miocene flooding events of western
Amazonia Science Advances 3 e1601693 httpsdoiorg101126
sciadv1601693
Jaramillo C Rueda M J amp Mora G (2006) Cenozoic plant diversity in
the Neotropics Science 311 1893ndash1896 httpsdoiorg101126sc
ience1121380
Jordan G amp Goldman N (2012) The effects of alignment error and
alignment filtering on the sitewise detection of positive selection
Molecular Biology and Evolution 29 1125ndash1139 httpsdoiorg10
1093molbevmsr272
Kass R E amp Raftery A E (1995) Bayes factors Journal of the American
Statistical Association 90 773ndash795 httpsdoiorg101080
01621459199510476572
Katoh K Misawa K Kuma K amp Miyata T (2002) MAFFT A novel
method for rapid multiple sequence alignment based on fast Fourier
transform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg10
1093nargkf436
Losos J B amp Ricklefs R E (2009) Adaptation and diversification on
islands Nature 457 830ndash836 httpsdoiorg101038nature07893
Luebert F Hilger H H amp Weigend M (2011) Diversification in the
Andes Age and origins of South American Heliotropium lineages
(Heliotropiaceae Boraginales) Molecular Phylogenetics and Evolution
61 90ndash102 httpsdoiorg101016jympev201106001
Luebert F amp Weiged M (2014) Phylogenetic insights into Andean plant
diversification Frontiers in Ecology and Evolution 2 1ndash17
Manchester S R Lehman T M amp Wheeler E A (2010) Fossil palms
(Arecaceae Coryphoideae) associated with juvenile herbivorous dino-
saurs in the Upper Cretaceous Aguja Formation Big Bend National
Park Texas International Journal of Plant Sciences 171 679ndash689
httpsdoiorg101086653688
Matzke N J (2014) Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades
Systematic Biology 63 951ndash970 httpsdoiorg101093sysbio
syu056
Miller M A Pfeiffer W amp Schwartz T (2010) Creating the CIPRES
Science Gateway for inference of large phylogenetic trees In Pro-
ceedings of the gateway computing environments workshop (GCE) New
Orleans USA pp 1-8
Montes C Cardona A Jaramillo C Pardo A Silva J C Valencia V
Ni~no H (2015) Middle Miocene closure of the Central American
Seaway Science 348 226ndash229 httpsdoiorg101126scienceaaa
2815
Moore B R Hohna S May M R Rannala B amp Huelsenbeck J P
(2016) Critically evaluating the theory and performance of Bayesian
analysis of macroevolutionary mixtures Proceedings of the National
Academy of Sciences of the United States of America 113 9569ndash9574
httpsdoiorg101073pnas1518659113
Morley R J (2003) Interplate dispersal paths for megathermal angios-
perms Perspectives in Plant Ecology Evolution and Systematics 6 5ndash
20 httpsdoiorg1010781433-8319-00039
Nee S Holmes E C May R M amp Harvey P H (1994) Extinction
rates can be estimated from molecular phylogenies Phylosophical
Transactions of the Royal Society B 344 77ndash82 httpsdoiorg10
1098rstb19940054
Nieto-Blazquez M E Antonelli A amp Roncal J (2017) Historical bio-
geography of endemic seed plant genera in the Caribbean Did
GAARlandia play a role Ecology and Evolution 7 10158ndash10174
httpsdoiorg101002ece33521
Nylander J A (2004) MrAICpl Program distributed by the author Upp-
sala Sweden Evolutionary Biology Centre Uppsala University
OrsquoDea A Lessios H A Coates A G Eytan R I Restrepo-Moreno S
A amp Cione A L Jackson J B (2016) Formation of the Isthmus
of Panama Science Advances 2 e1600883 httpsdoiorg101126
sciadv1600883
Oleas N Jestrow B Calonje M Peguero B Jimenez F Rodrıguez-Pe~na R Francisco-Ortega J (2013) Molecular systematics of
threatened seed plant species endemic in the Caribbean Islands The
Botanical Review 79 528ndash541 httpsdoiorg101007s12229-013-
9130-y
Penn O Privman E Ashkenazy H Landan G Graur D amp Pupko T
(2010) GUIDANCE A web server for assessing alignment confidence
scores Nucleic Acids Research 38 W23ndashW28 httpsdoiorg10
1093nargkq443
Rabosky D L (2014) Automatic detection of key innovations rate
shifts and diversity-dependence on phylogenetic trees PLoS ONE 9
e89543 httpsdoiorg101371journalpone0089543
Rabosky D L Mitchell J S amp Chang J (2017) Is BAMM flawed The-
oretical and practical concerns in the analysis of multi-rate diversifi-
cation models Systematic Biology 66 477ndash498 httpsdoiorg10
1093sysbiosyx037
Rambaut A Suchard M A Xie D amp Drummond A J (2014) Tracer
v16 Retrieved from httpbeastbioedacukTracer
Ree R H amp Smith S A (2008) Maximum likelihood inference of geo-
graphic range evolution by dispersal local extinction and cladogene-
sis Systematic Biology 57 4ndash14 httpsdoiorg101080
10635150701883881
CANO ET AL | 11
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats
Ricklefs R amp Bermingham E (2008) The West Indies as a laboratory of
biogeography and evolution Philosophical Transactions of the Royal
Society B Biological Sciences 363 2393ndash2413 httpsdoiorg10
1098rstb20072068
Roncal J Zona S amp Lewis C E (2008) Molecular phylogenetic studies
of Caribbean Palms (Arecaceae) and their relationships to biogeogra-
phy and conservation The Botanical Review 74 78ndash102 httpsdoi
org101007s12229-008-9005-9
Ronquist F Teslenko M van der Mark P Ayres D L Darling A Heuroohna
S Huelsenbeck J P (2012) MrBayes 32 Efficient bayesian phylo-
genetic inference and model choice across a large model space System-
atic Biology 61 539ndash542 httpsdoiorg101093sysbiosys029
Rull V (2011) Neotropical biodiversity Timing and potential drivers
Trends in Ecology amp Evolution 26 508ndash513 httpsdoiorg101016j
tree201105011
Salamanca Villegas S van Soelen E E Tunissen M L Flantua S G A
Ventura R Roddaz M Hoorn C (2016) Amazon forest dynam-
ics under changing abiotic conditions in the early Miocene (Colom-
bian Amazonia) Journal of Biogeography 43 2424ndash2437 httpsdoi
org101111jbi12769
Santiago-Valentin E amp Olmstead R G (2004) Historical biogeography
of Caribbean plants Introduction to current knowledge and possibili-
ties from a phylogenetic perspective Taxon 53 299ndash319 httpsd
oiorg1023074135610
Schulte P Alegret L Arenillas I Arz J A Barton P J amp Bown P R
Willumsen P S (2010) The Chicxulub asteroid impact and mass
extinction at the Cretaceous-Paleogene boundary Science 327
1214ndash1218 httpsdoiorg101126science1177265
Stadler T (2011a) Mammalian phylogeny reveals recent diversification
rate shifts Proceedings of the National Academy of Sciences 108
6187ndash6192 httpsdoiorg101073pnas1016876108
Stadler T (2011b) Simulating trees with a fixed number of extant spe-
cies Systematic Biology 60 676ndash684 httpsdoiorg101093sysb
iosyr029
Thomas R amp De Franceschi D (2012) First evidence of fossil Cryoso-
phileae (Arecaceae) outside the Americas (early Oligocene and late
Miocene of France) Anatomy palaeobiogeography and evolutionary
implications Review of Palaeobotany and Palynology 171 27ndash39
httpsdoiorg101016jrevpalbo201111010
van Ee B W Berry P E Riina R amp Gutierrez Amaro J E (2008)
Molecular phylogenetics and biogeography of the Caribbean-centered
Croton subgenus Macoroton (Euphorbiaceae ss) The Botanical
Review 74 132ndash165
Yang Z amp Rannala B (2006) Bayesian estimation of species divergence
times under a molecular clock using multiple fossil calibrations with
soft bounds Molecular Biology and Evolution 23 212ndash226 httpsd
oiorg101093molbevmsj024
Zachos J C Dickens G R amp Zeebe R E (2008) An early Cenozoic
perspective on greenhouse warming and carbon-cycle dynamics Nat-
ure 451 279ndash283 httpsdoiorg101038nature06588
Zona S (1990) A monograph of Sabal (Arecaceae Coryphoideae) Aliso
12 583ndash666 httpsdoiorg105642aliso
BIOSKETCH
Angela Cano is interested in understanding how ecological and
evolutionary processes shape tropical forest biodiversity She is
mainly focused on the Neotropical region and uses palms as a
model to unravel the historical assembly of its flora She con-
ducted her PhD at the University of Geneva and the Botanical
Garden of Geneva in collaboration with the Antonelli Lab at the
University of Gothenburg
Author contributions MP FWS AC AA and CDB con-
ceived the ideas AC and FWS collected the data AC MLS-
S and CDB analysed the data and AC MP CDB AA and
FWS participated in the writing of the manuscript
SUPPORTING INFORMATION
Additional Supporting Information may be found online in the
supporting information tab for this article
How to cite this article Cano A Bacon CD Stauffer FW
Antonelli A Serrano-Serrano ML Perret M The roles of
dispersal and mass extinction in shaping palm diversity across
the Caribbean J Biogeogr 2018001ndash12 httpsdoiorg
101111jbi13225
12 | CANO ET AL
View publication statsView publication stats