NREM/ZOOL4464–OrnithologyDr.TimO’ConnellLectures12–1413–17February,2017•Cladistics–weightstheimportanceofsometraitsoverothers.Ancestraltraitslike“twolegs”arenotthatusefulforclassifyingbirds–theyallhavetwolegs.Moreimportantareshared,derivedcharacters(“synapomorphies”)thatindicatehomologousstructure.Strivesfor100%objectivityincomparingnumbersofsynapomorphiesamonggroups.•Phenetics-DEGREEofdivergenceisparamount.Taxaaregroupedbygrossoverallsimilarity(morphology)•Cladistics-TIMEsincedivergenceisparamount.Itdoesn’tmatterwhattheylooklikeoverall,it’sevidenceforancestrythatreallycounts(inferredgenetics)•Thenumberofshared,derivedcharacters(synapomorphies)isimportantindeterminingancestry•Ex)humansaren’tcloselyrelatedtochimpsbecausebothspecieshavehairandnursetheiryoung[allmammalsdothat],butratherbecausebothhave5-fingeredhandswithopposablethumbs,stereoscopicvision,bigbrains,notails,bunodontdentition,etc.•It’sthethingswehaveincommonwithchimpsthatwedon’thaveincommonwithothermammalsthatprovidethemostinsight.•Allgroups(“clades”)shouldbeMONOPHYLETIC•Monophyleticgroup:allmembersaredescendedfromasinglecommonancestor;alldescendantsofthatancestorareintheclade•Soundssilly,butthishashugeimplicationsforunderstandingwhatmakesabird,abird.

Considerthisphylogenetictree,acladogram.Speciesaisthecommonancestorofspeciesd,e,g,h,k,andl.

Taxon1ismonophyletic:Asingle,commonancestor(b)gaverisetoallspeciesinthetaxonwithnodescendantsplacedinanyothertaxon.Ex)AllbearsareinthefamilyUrsidae;thereisnothingdescendedfrombearsthatisinanyotherfamily.

Taxon2

ispolyphyletic:Membersofthistaxonaredescendantsofmorethanonecommonancestor,inthiscase,both(c)and(f)areancestral.

ThekingdomPlantaeispolyphyleticbecausefloweringplantsandmossesarebothplantsbuttheyarosefromdifferentancestors.

Taxon3isparaphyletic:Inthiscase,thetaxonexcludesspeciesthatshareacommonancestorwiththeoneormorespeciesinthetaxon.TheClassReptiliaisparaphyleticbecauseitdoesnotincludemammalsorbirdsbothofwhicharedescendedfromreptiles.

MethodsofSystematics•Phenetics–lumpsorganismsincategoriesbasedondegreesofoverallsimilarity,withnoattempttoreflectevolutionaryhistory.•Cladistics–weightstheimportanceofsynapomorphiesoverothertraits.•Evolutionarysystematics–weightshomologoustraitsevenfurtherthancladistics,usingthelogicthatsometraitsmaybesharedandderivedbutirrelevanttothelifehistory.Ifthefeaturedoesn’tplayakeyroleinfitness,whyuseitforclassification?•Cladisiticrevolution–biochemicalgenetics:directlycomparestheamountofgeneticdivergencebetweengroups,i.e.,theHolyGrailofsystematics.

DNA/DNAhybridization

•DNA/DNAhybridization(fromFredSheldon’sworkonherons):•a=GTBH/GTBH,b=GTBH/GREG,c=GTBH/AMBI,d=GTBH/GLIBDependingonwhatDNAsourceisused,hybridizationandsimilarapproachescanbeusedtoillustraterelationshipswithinaclade:

...Ortheycouldillustrateeverythingfrombroadrelationshipsamongorderstoactualgeneticdiversitywithinasinglepopulation.Here’sanexampleofthelatter:Zink,R.M.,A.W.Jones,C.C.Farquhar,M.C.Westberg,andJ.I.GonzalezRojas.2010.ComparisonofmolecularmarkersintheendangeredBlack-cappedVireo(Vireoatricapilla)andtheirinterpretationinconservation.TheAuk127:797–806.•Collaborators:UniversityofMinnesota,ClevelandMuseumofNaturalHistory,TexasParksandWildlifeDepartment,IndependentUniversityofNuevoLeon•LeadauthorBobZink.Activeinmolecularsystematicsofbirdsforatleast25years;aleaderinexploringspecies

conceptsinevolutionarybiology.TheBlack-cappedVireo•EndemicsongbirdofoakscrubandsavannaintheSouthernPlains.•Lossofhabitat(firesuppression,urbanization)andbroodparasitismbyBrown-headedCowbirdcausedpopulationdeclinein20thCenturyandisolationofbreedingoccurrences.Bottomedoutat<200pairsinU.S.by1990s.•NownestsonlyinnorthernMexico(twostatesthere),centralTexas,andsouthwesternOklahoma.(WintersinsouthwesternMexico.)•Listedas“endangered”inU.S.andMexico,“vulnerable”byIUCN.Nowabout1000pairs

inOK.•Conservationgeneticsissue:ifbreedingoccurrencesareisolatedfromeachother,doesthismeanthatgeneflowisrestricted?•Geneflow–transferofallelesfromonepopulationtoanother.Geneflowisrestrictedinallopatric(“othercountry”)populations(thoseseparatedbysomebarrier)andgenerallyprevalentinsympatricpopulations.Reducedgeneflowinallopatricpopulationsconsideredfirststeptowardreproductiveisolation,i.e.,speciationorextinction.IsolatedoccurrencesofBlack-cappedVireo:•Ifgeneflowisrestricted,thiscouldleadtogeneticbottlenecksinseparateoccurrences.•Geneticbottleneck–eventleadingtosignificantreductioningeneticdiversitywithinapopulation.Reduceddiversitycanresultininbreedingandinabilitytorespondtonewselectivepressures.ConservationGenetics•Howdoweexaminethedegreeofgeneticdiversityinapopulation?•GenesaresequencesofnucleotidebasepairsatspecificlocationsinaDNAstrandthatcodeforsometrait,e.g.,eyecolorortheproductionofanenzyme.

•Allelesaredifferentformsofgenes,e.g.,blueeyesvs.browneyesorvariablestructuresofanenzymethatstillcatalyzesthesamereaction.•Polymorphism–twoormorediscretephenotypesinasympatricpopulation.Examplesincludetan-stripedandwhite-stripedWhite-throatedSparrows,humanbloodtypes,etc.•Examinesourceofpolymorphisms!•e.g.,alloenzymes–generallyconservative(lowmutationrate)sopolymorphismscanbestrongindicatorofevolutionarychange.•Microsatellites–repeatedsequencesof1–6basepairsofDNA.Highmutationratesresultinlotsofpolymorphisms–inotherwords,therearelotsofdifferentallelestoexamineinamicrosatellite.Thesecanindicategeneticdiversitywithinpopulationsofthesamespecies.•MitochondrialDNA–yep,mitochondriahavetheirownDNA–canalsoserveasusefulgeneticmarkers,butlimitedbythesizeofthegenomeandonlyinheritedfromthematernalline.Candistinguishamongindividuals.Zinketal.2010:Introduction–•SomeauthorsquestioningtheuseofmitochondrialDNA(mtDNA)•ZinkhasdatatosuggestthatforbirdsitmatchesupwellwithsimilarstudiesofnuclearDNA(e.g.,microsatellites).•Ifanything,microsatellitesmightbeunreliableforsomeapplicationsbecausetheymutatesofrequently.•Goal:“analysisofmolecularvariance”orAMOVA–toidentifydifferenceswithinpopulationsthathavebeenisolated.a.k.a.“geneticstructure”•Inthiscase,useBlack-cappedVireoasamodeltotestmtDNAvs.microsatellitesinAMOVA•PreviousstudyofallozymesshoweddifferentiationoftheOklahomapopulation–willnewanalysisusingmicrosatellitesandmtDNAconfirmthis?Methods–•ObtainedfeathersfrombirdsinOK,TX,andMexico(n=108)• ExtractedDNAfromfeathersandrananalysisonDNAResults-•FrommtDNA,only2of9analysesshoweddivergence.•Onbalance,noevidenceforgeneticstructuring•Frommicrosatellites,moreevidenceforstructuring:“isolationbydistance”,butonlyforabout2.4%ofthemolecularvariance.•Inotherwords,98%ofthevariancenotexplainedbygeography.

Discussion-•FrommicrosatellitesandmtDNA,<3%ofgeneticvariationexplainedbylocation=lowevidenceofgeneticstructuring.•Previousstudiesdemonstratinggeneticstructureusingmorerestricteddatahaveconcludedthatemphasisinconservationshifttopromotingdispersalamongpopulations.•Zinketal.concludethatdispersalishappeningwithouthumanintervention.•Statisticalsignificanceinconservationgeneticsdoesnotnecessarilyleadtobiologicalsignificanceforconservation.•Thus,noneedtoestablishcorridorsto“link”thedisjunctpopulations.Despitethedistancesbetweentheseparateoccurrences,geneflowistakingplace.Okay,sowhataboutrelationshipsatreallybroadlevels?Modernhierarchyoflifeonearth:•Domain•Kingdom•Phylum(plural“phyla”)•Class•Order•Family•Genus(plural“genera”)•Species(plural“species”)

WithinAnimalia•PhylumChordata•SubphylumVertebrata•ClassAves

Amongbirds,onebigandobviousanatomicalsplithasbeenthestructureofthebodypalateoftheuppermandible.Themoreancestralcondition(“paleognath”)isfoundinostriches,emus,kiwis,elephantbirds,moas,rheas,andthechicken-liketinamous.Allothermodernbirdspecies(likenearly10,000species)shareamorederivedpalatestructure(“neognath”).That’sfine,butdowereallyhaveenoughanatomicaldifferencestounderstandtheevolutionaryrelationshipsamongtheAves?Toearrangement,featherstructure,nataldevelopment–thesetraditionalcomparativeapproacheshaveprovidedabasicunderstandingofrelationships,butthoserelationshipshaveinsomecasesbeencalledintoquestionbyDNA-DNAhybridizationstudies,notablythatofSibleyandAhlquistin1990.Thatjustbegsthequestion:howdoweknowthatSibleyandAhlquistdidanybetter?Ourbestopportunitytosolvetheproblemwouldbetocompareentireaviangenomes...TheAvianPhylogeneticsConsortiumrecentlypublishedaseriesofpapersthatconfirmsomelong-heldsuspicionsaboutaviansystematics,andprovidesomesurprisestoo.Morethan200scientistsat80researchinstitutionshavecontributedtothiscolossalstudyinwhichthewholegenomesof48specieswereanalyzedandcompared.Thosespeciesrepresentedall32Neognathordersand2(ofthe5)Paleognathordersforthemostcompletepictureofavianphylogeneticsyet.

6

Theresultslookabitlikethis:

Thebigsplits–AvesPaleognathae–ostriches,emus,tinamous,etc.Neognathae–everythingelseNeognathaeGalloanseres–chickenyandduckythingsNeoaves–everythingelseNeoavesColumbea–pigeonythings(includesgrebesandflamingoes!)Passerea–everythingelsePassereaTheremaining22ordersofbirds,mostlyfallingalongtraditionallinesoftaxonomy

7

Tobegintogetyoucomfortableinthinkingaboutordersandfamiliesofbirds,herearesomeplatesfromtheHandbookoftheBirdsoftheWorld:

8

9

Modernhierarchyoflifeonearth:•Domain•Kingdom•Phylum(plural“phyla”)•Class•Order•Family•Genus(plural“genera”)•Species(plural“species”)•Prokaryotes–nonucleusandnosubcellularorganelles.Theseareexceedinglytiny0.1–10micronsdiameter.•Eukaryotes–largercells(10–100microns)withDNAcontainedinanucleusandnumerousmembrane-boundorganelleslikemitochondria,Golgiapparatus.FourkingdomsoftheEukarya:•Protista-mostunicellular,hetero-orautotrophicorboth•Plantae-multicellular,photosyntheticautotrophs•Fungi-multicellularheterotrophsthatfeedbyabsorption•Animalia-multicellularheterotrophsthatfeedbyingestionWithinAnimalia•PhylumChordata•SubphylumVertebrata•ClassAvesPaleontologistPhilCurrie,commentingonrecentfossilfindsinChinaofdinosaurswithfeathers:"Thisshowsthatdinosaursarenotextinct,butarewell-representedby10,000speciesofbirds."Whatdidhemean?Arebirdbirds,orarebirdsreallydinosaurs?Theissue:•Birdsareobviouslyalliedwithreptiles,andspecificallytodinosaurs.Ancestryambiguous,however.

10

•DidbirdsdescendfromancientreptilesthatwereNOTdinosaurs,ordidbirdsdescendDIRECTLYFROMdinosaurs?•Ifthelatter,thenbirdsaretechnicallyconsidereddinosaursaccordingtoamoderncladisticanalysis.Thatis,dinosaursdidNOTdieoutattheendoftheCretaceous!Adaptiveradiation-processthroughwhichonetaxongivesrisetomanyothersthatexploitavailableniches.WeneedtogobacktothePaleozoic–theriseoftheTetrapods!~450millionyearsago(MYA),bonyfishwithcartilaginousraysintheirfinsappear.~420(blazeit!)MYA,somefishdevelopfleshyfinswithboneandmuscleinside,e.g.,Coelocanth.~410MYA,some“lobe-finned”fishdevelopastructureofoneproximallimbbonearticulatingwithtwodistallimbbonesineachlimb.Thisisthebeginningofhumerus-radius/ulna.~385MYA,Tiktaalikshowsadevelopmentofthepectoralgirdlesufficienttobearitsweightwithoutthebuoyancyofwater!~380MYA,Acanthostegahasdigitsattheendofits4limbs.~370MYA,amphibiansappear–5digitson4limbs–thesearetheancestralTetrapods.KingdomAnimalia,PhylumChordata,(SubphylumVertebrata),ClassReptilia–adaptiveradiationofreptilesintheMesozoicEra,~250–65mya.Fromthebasalstockofreptiles(cotylosaurs),atleastSIXmajorgroupsdeveloped:TurtlesPlesiosaurs(long-neckedmarinereptiles)Icthyosaurs(dolphin-shapedmarinereptiles)Pelycosaurs(ancestraltothetherapsidsfromwhichwemammalsdescended)Eusuchians(ancestraltolizards,snakes,andthetuatara)Pseudosuchians(a.k.a.“thecodonts”,so-namedbecausetheirteethsitinindividualsocketsinthejaw).Thepseudosuchiansareancestraltocrocodilians,pterosaurs(flyingreptiles),andthedinosaurs–thegroupthatunderwentoneofthemostdramaticadaptiveradiationstheworldhaseverseen.

11

Dino-diversity:Thedinosaurradiationledtothedevelopmentofmanywildlydifferentforms.Alldinosaurshadtheirlimbsrotatedtosupportthebodyfrombeneath–likemammallimbs–ratherthansplayedouttothesidesasinlizards,turtles,andcrocodilians.Significantly,dinosaursradiatedintoancestralquadrapedalformsandderivedbipedalforms.Thebigsplitindino-diversityinvolvestheorientationofthebonesinthepelvis:ilium,ischium,andpubis.IntheORNITHISCHIANS,thepubisbonepointsbackwards,asitdoesinmodernbirds(althoughaswe’llsee,birdsdidn’tdescendfromtheornithischians).

TheornithischiansincludesuchfamiliardinosaursasStegosaurus,Ankylosaurus,theceratopsianslikeTriceratops,andthehadrosaurs,i.e.,the“duck-billeddinosaurs”likeTrachodon.

Iguanodon

Stegosaurus

OppositetheornithischiansweretheSAURISCHIANS,the“lizard-hipped”dinosaurswiththepubisbonepointedforward:TheSaurischiansradiatedintothemassivelong-neckedsauropodslikeBrachiosaurusandthemeat-eating,bipedaltheropods.ThebigtheropodslikeTyrannosauruswerethe“carnosaurs”andthelittleviciousoneslikeVelociraptorwerethe“coelurosaurs.”

12

Seismosaurus

Megalosaurus

Thestructureofmodernbirdshasbeendramaticallyshapedbythedemandsofefficient,poweredflight.Thatsaid,therearenumeroussimilaritiesbetweenbirdsanddinosaurs,especiallythosecoelurosaurs.That’stheissue:Didbirdsdescenddirectlyfromsomebasalstockofreptileslikethepseudosuchians,ordidtheyariselater,descendingdirectlyfromthecoelurosaurdinosaurs?Ifbirdsdescendeddirectlyfromthepseudosuchians,thentheprincipleofmonpohyleticismwoulddictatethatbirdsbeincludedwithreptilesintheclassReptilia.Ifbirdsdescendeddirectlyfromthecoelurosaurs,thenbirdsarenotjust“reptiles,”theyareaspecifictypeofreptile–dinosaurs!ThisisonlyreallyabigdealifweconsiderdinosaurstohavegoneextinctattheendoftheCretaceous.Ifbirdsaredinosaurs,thatmeansthatthedinosaursDIDNOTdieoutattheendoftheCretaceous;thousandsofthemarestillwithustoday.Toexaminethisissue,weneedtoconsidertheanatomyofbirdsandreptiles–specificallydinosaurs.

13

Tobegintoappreciatethestructureofbirds,weneedtohaveabasicunderstandingofskeletalstructureinanancestralreptile.ConsiderEuparkeria,agenusofTriassicpseudosuchianreptilesthatpredatethedinosaurs,fromabout345mya.

Let’slookatitsskeleton:AxialskeletonIncludesskull,allvertebrae(cervical,dorsal{thoracic,lumbar},sacralandcaudal,ribcage,andsternum.AppendicularskeletonIncludeslimbbonesplusscapula,coracoid,claviclesandpelvis.Euparkeria’sancestralconditionshowsalong,bonytail,teethinthejaw,atleast10pairsofribs,andinthelimbs,asolidbone(femurandhumerus)proximallyanddistallypairedbones(tibiaandfibulainthehindlimbs;radiusandulnaintheforelimbs)thatendinfeetwithfivedigits.

Arealtheropoddinosaur:Compsognathus.ThisisamuchmorederivedskeletonthanthatofEuparkeria.

14

Manyofabird’suniquefeaturesaremodificationsassociatedwiththedemandsforflight.Still,despitenumerousmodificationsforthedemandsofflight,birdsareremarkably“reptilian.”Scales,layeggs,singleurogenitalopening...FEATHERSarethekey:Ifit’sgotfeathers,thenit’sabird.Exceptionalbirds:Hoatzin-(extantinSouthAmerica)nestlingshaveclawsontheirwings.Hesperornisregalis:ACretaceousbirdthatwasstructurallysimilartoaloonorcormorant,thoughflightless.Itsbonybeakhadteeth.CharlesDarwinpublisheshis‘OriginofSpecies’inwhichhedescribeshistheoryofevolutionbynaturalselection-1859.Predictedbythattheory:“intermediate”formsinthefossilrecord(andaroundtoday).ThomasHenryHuxley,citingskeletalsimilaritiesbetweendinosaursandmodernbirdswasthefirsttopublishhisideathatbirdsdescendedfromdinosaurs.[Notjustreptiles,butspecificallydescendedfromthedinosaurs.]EnterArchaeopteryxlithographicain1862-afterHuxley’sproclamation:

SkeletonsofArchaeopteryx(left)andamodernpigeon(Columba)(right).

Skeletally,almostidenticaltosmallcoelurosaurs.Oneimportantdifference,though...Archaeopteryxhadfeathers.Fullyformedandmodernfeathers-includingasymmetricalvanesontheflightfeathersthatarepresumedtobeanadvancedcharactercompatiblewithflight.

15

Birdsandfeathereddinosaurs.ThesereconstructionsfromMatthewMartyniuk:Here’swhatourmostadvancedreconstructionsofArchaeopteryxsuggestitprobablylookedlike:AgroupofcoelurosaurscalledthemaniraptorswereskeletallysimilartoArchaeopteryx:sickle-clawtoe,semi-lunatecarpal,posteriororientationofpubis,largeeyes&braincase,hollowbones,3-fingeredhand,4-toedfoot,fusedclavicles,bladelikescapula,secondarybonypalate,and...Feathers!

Someofthesynapomorphiesbetweenmodernbirds,Archaeopteryx,andmaniraptors:*Secondarypalate*3-fingeredhand,4-toedfoot*Semi-lunatecarpal*Furcula*Bladelikescapula

*Hingelikeankle-nolateralmovement*Highmetabolism*Bigeyes,bigbrains*FEATHERS!

16

BasedmostlyonspectacularfossilfindsfromquarriesinChina,wenowhaveatleast13differentgeneraofcoelurosaursknowntohavehadfeathersor“protofeathers”andmanyotherspecies,e.g.,Velociraptor,aresuspectedofhavingbeenfeatheredaswell.

Sinornithosaurus:Gigantoraptorandrelatedfeathereddinosaurs(CretaceousPeriod):Here’swhatVelociraptorprobablyreallylookedlike:

So,accordingtoJohnOstrom,PhilCurrie,JackHorner,BobBakker,andeverythinkingcladistoutthere,birdsmustshareacommonancestorwiththecoelurosaurs,i.e.,birdsaredescendedfromdinosaursandthereforeAREdinosaurs.

Asmall,butvocalgroupstandsinopposition:•AlanFeduccia,SankarChatterjee,PeterDodson•Concernedabouttimelineprimarily,butalsodisputesomeofthefeatheredfossils:•ArethoseREALLYfeathers?•Whichspecificdigitswerelost/retainedonthe3-fingeredhand?•PresenceoffeathersonALLmaniraptorsisstillconjectural.•Maybebirdsaren’tdinosaurs,maybethosefeathereddinosaursarereallyflightlessbirds...Areabirds’handbonesdigits2,3,and4or–likealltheropods–1,2,and3?

17

Timelineofmodernbirds,Archaeopteryx,andfeatheredmaniraptors:•Modernbirdsappear~60mya•Archaeopteryx~150mya•Earliestcoelurosaurs~165mya•Feathereddinosaurs,“raptors”~135-80mya•IfArchaeopteryxisolderthantheCretaceousfeathereddinosaurs,andunequivocallyatruebird,thentheREALintermediatereptile/birdmustbemucholderthanArchaeopteryx!•Contrarytothemediafrenzy,NONEofthefeathereddinosaursdiscoveredtodatewasancestraltobirds!Themediaimpressioncreatedbythesediscoveriesisthatthefeathereddinosaurswereancestorstobirds.Thatcan’tbebecauseArchaeopteryxfromtheJurassicPeriodwasalreadymorebirdlikethatthefeathereddinosaursthatappearedlater.Arethereanycandidatesforbird-likereptilesmucholderthanArchaeopteryx?Longisquama,Triassicage-220mya.Thislizard-likecreaturewasNOTadinosaurORabird,butithadfeather-likeprojectionsgrowingoutofitsspine,andprobablyglidedamongtrees.ItshowsfewsynapomorphieswithArchaeopteryx,butdoesillustratethatfeatherscouldhaveevolvedmorethanonce,andmuchearlierthancurrentlypresumed.ButnooneseriouslyconsidersLongisquamaancestraltobirdsbecauseitisotherwisesodifferentinstructureandsomuchmoresimilartolizards.Themostwidelyheldancestryofbirdsthesedayslookssomethinglikethis:

Evenmorerecentdiscoveries,however,starttofillinsomeoftheblanks:olderthanArchaeopteryx.•Manymorefeathereddinosaursnowdiscovered,includinghundredsofindividualspecimens•Xiaotingia,155MYA

18

•Epidexipteryx,160MYA•Anchiornis,160MYA•Unlikelythatallthebird/coelurosaursynapomorphiesaremistakes,lies,orconvergence•Tosuggestthatcoelurosaursarederivedbirdsignoresthesynapomorphiesbetweenthefeatheredandnon-featheredtheropods-thatis,ifComposgnathuswasabird,thenTyrannosauruswastoo.•Littleevidenceforanearlier“proto-bird”thanArchaeopteryx-Longisquamaistoodistanttoforgeadefensiblelinktomodernbirds•Parsimonyandcladisticsdictatethatbirdsareindeed,livingdinosaurs.