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Ecology and Evolution. 2017;7:9935–9953. | 9935www.ecolevol.org
Received:8March2017 | Revised:27July2017 | Accepted:19August2017DOI: 10.1002/ece3.3420
O R I G I N A L R E S E A R C H
Ancestrality and evolution of trait syndromes in finches (Fringillidae)
Jean-François Ponge1 | Dario Zuccon2 | Marianne Elias3 | Sandrine Pavoine4 | Pierre-Yves Henry1 | Marc Théry1 | Éric Guilbert1
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,providedtheoriginalworkisproperlycited.©2017TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.
1MuséumNationald’HistoireNaturelle,Mécanismesadaptatifsetévolution(MECADEVUMR7179),SorbonneUniversités,MNHN,CNRS,Brunoy,France2MuséumNationald’HistoireNaturelle,ServicedeSystématiqueMoléculaire,Paris,France3MuséumNationald’Histoirenaturelle,InstitutdeSystématique,Évolution,Biodiversité(ISYEBUMR7205),CNRS,MNHN,UPMC,EPHE,SorbonneUniversités,Paris,France4MuséumNationald’HistoireNaturelle,Centred’ÉcologieetdesSciencesdelaConservation(CESCOUMR7204),MNHN,CNRS,UPMC,SorbonneUniversités,Paris,France
CorrespondenceJean-FrançoisPonge,MuséumNationald’HistoireNaturelle,CNRSUMR7179,Brunoy,France.Email:[email protected]
AbstractSpeciestraitshavebeenhypothesizedbyoneofus(Ponge,2013)toevolveinacor-relatedmannerasspeciescolonizestable,undisturbedhabitats,shiftingfrom“ances-tral” to “derived” strategies. We predicted that generalism, r-selection, sexualmonomorphism, andmigration/gregariousness are the ancestral states (collectivelycalled strategy A) and evolved correlatively toward specialism, K-selection, sexualdimorphism, and residence/territoriality as habitat stabilized (collectively called Bstrategy).Weanalyzedthecorrelatedevolutionoffoursyndromes,summarizingthecovariationbetween53traits,respectively, involvedinecologicalspecialization,r-Kgradient,sexualselection,anddispersal/socialbehaviorsin81speciesrepresentativeofFringillidae,abirdfamilywithavailablenaturalhistoryinformationandthatshowsvariabilityforallthesetraits.TheancestralityofstrategyAwassupportedforthreeofthefoursyndromes,theancestralityofgeneralismhavingaweakersupport,exceptforthecoregroupCarduelinae(69species).ItappearedthattwodifferentB-strategiesevolvedfromtheancestralstateA,bothassociatedwithhighlypredictableenviron-ments:oneinpoorlyseasonalenvironments,calledB1,withspecieslivingpermanentlyinlowlandtropics,with“slowpaceoflife”andweaksexualdimorphism,andoneinhighly seasonal environments, called B2, with species breeding out-of-the-tropics,migratory,witha“fastpaceoflife”andhighsexualdimorphism.
K E Y W O R D S
ancestralstate,evolution,Fringillidae,phylogeny,phylogeography,strategies
1 | INTRODUCTION
Ponge (2013) suggested that awide array of traits related to eco-logical niche requirements (e.g., specialistvs. generalist), life history(e.g., K- vs. r-selection), behavior (e.g., residents vs. dispersers, ter-ritorial vs. gregarious), and selection mode (e.g., sexual vs. naturalselection)co-evolvedalonggradientsofenvironmentalpredictability,formingtwosuitesofgeneralizedsyndromesorevolutionarystrate-gies.Accordingtothistheory,theancestralsuiteofsyndromes,here
collectivelycalledstrategyAandpreviouslycalled“barbarian”strategyinPonge(2013),includesgeneralism,r-selectedtraits,dispersiveness/gregariousness,andmoregenerallytraitsundernaturalselection (asopposed to sexual/social selection). It is associated with disturbedandunpredictableenvironments(Sallan&Galimberti,2015;Sheldon,1996).Conversely,oppositetraitmodalities(valuestakenbyagiventraitunderselection)includespecialism,K-selectedtraits,residence/territoriality,andtraitsundersexual/socialselection,herecollectivelycalled strategy B and previously called “civilized” strategy in Ponge
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(2013).They are predicted to evolve in stable environmentswith ahighlevelofexploitativecompetitionthroughcharacterdisplacement(Brown&Wilson,1956)andconvergence(Laioloetal.,2015),allowingspeciestosegregateandbecomefinelytunedtotheirenvironment.Given the number of evolutionary steps necessary for being finelytunedtotheenvironment(Poisot,Bever,Nemri,Thrall,&Hochberg,2011), traitmodalitiesof strategyBwould thusbe inderivedposi-tions inphylogenetic trees (seeRaia,Carotenuto,Passaro,Fulgione,&Fortelius,2012;foradiscussionaboutthederivedpositionofeco-logicalspecialization).Conversely,traitmodalitiesofstrategyAwouldthusbe inancestralpositionalongphylogenetictrees.Thissuggestsamacroevolutionarytrade-offbetweentheneedtomoveand/orre-produceandtheneedtospecializetostableresourcesandhabitats(seeBergetal.,2010;Bonteetal.,2012;Rottenberg,2007).Tropicallowlandareas,inparticulartropicalrainforests,knownfortheirgreaterstability and lower energetic cost for organisms compared to areaswithseasonalstress(Janzen,1967),arethusexpectedtoharbormoreB-strategytraits,thoughttobederived(Cardillo,2002).
Inthisarticle,wewanttotestsimultaneously,forthefirsttime,inamonophyleticgroup,thefollowinghypotheses:generalism,r-selection,natural selection,anddispersiveness/gregariousness (strategyA)areancestral and tend to shift towardderived (strategyB) attributes inthecourseofevolution(Hypothesis1),andthesefourtraitsyndromesevolvecorrelatively(Hypothesis2).Atlast,wehypothesizethatstateBtraitsarefavoredbytwokindsofpredictableenvironments:stableandbenigntropicalenvironmentsfavorstateBtraitsonly,whilestablebutseasonalorharshenvironmentsfavoracombinationofstateAandstateBtraits (Hypothesis3).Totestthesehypotheses,wechosetoworkwithbirdsbecausetheirtraitsareparticularlywell-documented,thanks toa long traditionofnaturalhistorydocumentationbyorni-thologists(Schmeller,Henle,Loyau,Besnard,&Henry,2012).Wese-lected thebird familyFringillidae (i.e., true finches) because (1) it isdistributedworldwide, (2) it isknownfor itswiderangeofvariationin termsofecological specialization, lifehistory, social/dispersalbe-havior,andsexualdimorphism(Clement,Harris,&Davis,2011),and(3)itsphylogenyiswell-establishedonthebasisofrepresentativesofallexistinglineages(Zuccon,Prŷs-Jones,Rasmussen,&Ericson,2012).Thisbird family is agoodmodel to follow theevolutionofmultiplesuitesoftraits,asattestedbyseveralstudiesperformedoncarduelinefinches (Badyaev,1997a,b,c;Badyaev&Ghalambor,1998;Badyaev,Hill,&Weckworth,2002).
2 | MATERIAL AND METHODS
2.1 | Data collection and preparation
TheliteratureonFringillidae(153references,AppendixS1)wasusedtocollectthenecessarynaturalhistorydata(AppendixS2).Fifty-threevariables were documented (Appendix S3). For each quantitativevariable (measurements, countdata)andeachspecies,weused theweightedarithmeticmeanvalueacrossallavailabledata.Qualitativedata (coded as “Yes” or “Yes minus” in Appendix S2) were codedas1for thepresenceof thecharacter,0for itsabsence,0.5for its
partialpresence).Whenthesamecharacterexhibiteddifferent traitmodalities (e.g., foraging height), datawere scored according to anarbitrary scale (e.g., foragingheightwas scored1 for ground, 2 forshrubs,3fortrees).Thevarianceofthesenumericalvalues(weightedby their occurrence in literature)was complemented to 1 andwasused as synthetic index of specialization (e.g., foraging height spe-cialization inAppendixS3).Altitudinal specializationofagivenspe-cieswasmeasuredbydividing itsaltitudinal range (maximumminusminimumaltitude)bythemaximumaltitudefoundinourdataset(i.e.,4,950m)andcomplementingto1thisratio.Thesamemethodbasedonweightedoccurrencewasusedtomeasuretheintra-specificvari-abilityof abehavioral traitwhen it exhibiteddifferent traitmodali-ties(e.g.,breedingdispersionandmigration).Missingdata(20±23%of total records, Appendix S3) were interpolated according to anearest-neighbormethod(Holmes&Adams,2002)priortoPrincipalComponentAnalysis(PCA).
2.2 | Phylogenetic tree
The Fringillidae phylogeny by Zuccon etal. (2012) included 93 in-grouptaxaof205extantspecies(sensuDickinson&Christidis,2014),representingallmajor lineages,genera,andspeciesgroupsandwasbasedonacombinationofthreenuclearandtwomitochondrialgenes.Here,weused the substitution rates for a cladeofFringillidae, thedrepanids,obtainedbyLerner,Meyer,James,Hofreiter,andFleischer(2011), to time-calibrate the phylogeny of Fringillidae. Because 12species had <50% of scored ecological traits, they were excludedfromtheanalysis.Thetime-calibratedphylogenywasgeneratedwithBEAST1.8.0 (Drummond&Rambaut,2007),as implemented in theCIPRESScienceGateway(Miller,Pfeiffer,&Schwartz,2010).Weas-sumedanuncorrelatedmolecularclockmodel,aspeciationyuletreepriorandaGTR+ΓorGTR+Γ+Isubstitutionmodel(Posada&Crandall,2001),fornuclearormitochondrialgenes,respectively.MarkovchainMonteCarlo (MCMC) simulationswere run for100milliongenera-tionswithsamplingevery10,000generations.TheconvergencewasevaluatedinTracer1.6,andthemaximumcladecredibilitytreewassummarizedusingTreeAnnotatorv1.8.0(bothpackagesimplementedinBEAST),excludingthefirst25%treesasburn-in.
Thisphylogenywasusedforthereconstructionofancestralsyn-dromes, for the phylogenetic Principal ComponentAnalysis (pPCA)and formodelingcorrelationsbetweentransitions fromancestral toderivedstates,asexplainedinthefollowingsections.Thetreethatweobtainedcoversabout40%ofFringillidaediversity.Noglobalphylog-enyfortheentirefamilyisavailable,butanumberofcompleteoral-mostcompletephylogenieshavebeenpublishedforsomesubclades/genera, forexample,Pyrrhula (Töpferetal.,2011),Carpodacussensulato (Tietze, Päckert,Martens, Lehmann,& Sun, 2013),Haemorhous (Smith, Bryson, Chua,Africa, & Klicka, 2013), and Spinus (Beckman&Witt, 2015). We evaluated the representativeness of the familydiversity inourphylogenybyaqualitativecomparisonagainsta su-permatrixtree.UsingthedatasetusedbyZucconetal.(2012)asstart-ingpoint,weassembledasupermatrixforthreenuclear intronsandfivemitochondrial genes by comparisonwith the datasets of other
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published phylogenies and searching inGenbank for any additionalfinch sequence (Appendix S4). The supermatrix treewas estimatedbymaximumlikelihoodusingRAxMLversion7.0.3(Stamatakis,2006),applyingagenepartition,aGTR+Γ+Imodel,andrandomstartingtree,withα-shapeparameters,GTR-rates,andempiricalbasefrequenciesestimatedandoptimizedforeachpartition.Nodalsupportwasesti-matedusing100bootstrapreplicates.
Wecalculatedphylogeneticdistancesbetweentwospeciesinthesupermatrix treeas thesumofbranch lengthson thesmallestpaththatconnects thetwospecies.Nextwecalculatedthemeanphylo-geneticdistance (MPD)betweentwospeciesamongthe81speciesselectedforouranalysis.Weanalyzedwhethertheselectedspeciesweremorephylogeneticallyclusteredthanexpectedrandomlyusinganullmodel.Wesimulated1,000nullcommunitiesbyselectingran-domly81speciesinthesupermatrixtree(outgroupexcluded).Thep-value (quantile)wascalculatedastheproportionoftheMPDofthenull communities thatwere lower than theobservedMPD.Weob-tainedobservedMPD=0.319andp=.837.Ourselectionof81spe-ciesthereforerepresentsarandomsampleofFringillidaephylogeneticdiversity.
2.3 | Construction of syndromes
Weselectedfoursetsofvariablesthattogetherdescribeacommonlifehistory,ecological,orbehavioralpattern,whichwecallsyndromesaccordingtoSih,Bell,andJohnson(2004).Eachonedescribeseitherr-K-gradient,ecologicalspecialization,sexualselection,ordispersal/social behavior (Appendix S3). Tomaximize independencebetweensyndromes,wetookcarenottoincludethesamevariableinthecal-culation of different syndromes. For each syndrome, all attributedvariableswere submitted to PCA,with Spearman’s coefficient as ameasureof correlation, to extract the correlated variationbetweendominantvariables,thatis,thefunctionsoftheprincipalcomponents.Ideally,onlythefirstprincipalcomponentwouldhaveadistinctivelyhigheigenvalue (Sihetal.,2004)andcouldbeusedas singleproxyforecologicalspecialization,r-Kgradient,sexualselection,anddisper-sal/socialbehavior,respectively.Foreachsyntheticvariable,speciesweresplit intotwogroupsbyk-meansclustering (Steinhaus,1956),maximizingtheratioofbetween-groupversuswithin-groupvariance.Thesetwogroupswereconsideredastwolevelsofeachsyndrome,whichcouldthenbetreatedasadiscretevariable.CalculationswereperformedusingXLSTAT®forExcel®(Addinsoft®,Paris).
2.4 | Reconstruction of the ancestral states of syndromes
Reconstructionofancestralstates(H1)andtestforcorrelatedevolu-tionofthefoursyndromes(H2)wereperformedusingBayesTraits2.0(Pagel&Meade,2006;Pagel,Meade,&Barker,2004).Specifically,foreachsyndromeancestral statesand transition ratesbetweenstateswere estimatedbymaximum likelihood (H1). To test for correlatedevolutionofthefoursyndromes(H2),foreachpairofsyndromeiandj wecomputedthetransitionratesbetweenstatesofsyndromeiunder
1)amodelwhere transitions in syndrome iwere independent fromtransitionsinsyndromej(independentmodel)and2)amodelwheretransitionsinsyndromeidependedontransitionsinsyndromej (de-pendentmodel, Pagel&Meade, 2006).We then selected the bestmodelbyperformingalikelihoodratiotest(LRT).Iftraitsevolveunderadependentmodel,thismeansthattheirevolutioniscorrelated,inawaydepictedbytheestimatedtransitionrates(seesection3).
2.5 | Phylogenetic principal components analysis (pPCA)
Thefoursyndromes(thefirstprincipalcomponentsofthefouroriginalPCAs)wereusedascontinuousvariablesinapPCA(Jombart,Pavoine,Devillard,&Pontier,2010),allowingtodiscernaphylogeneticsignalcommontoallfoursyndromes.Phylogeneticsignal(autocorrelation)wastestedoneachsyntheticvariablebyAbouheif’s test (Abouheif,1999;Pavoine,Ollier,Pontier,&Chessel,2008).ThesemethodswereperformedusingtheadephylopackageofR(RCoreTeam,2016).Thereconstructionof ancestral statesof the four syndromes suggestedthatstrategyBshouldbesubdividedintwogroups.Therebythefirstthree components of pPCAwere used to split the species in threestrategiesA,B1,andB2byk-meansclustering.
2.6 | Association of syndromes with tropical affinity
The tropical affinity of species was determined according to geo-graphical records (AppendixS2).Specieswereconsideredashavingatropicalaffinitywhenmorethanhalfoftheirdistributionareawaslocatedinthetropics.Totesttheassociationofeachsyndromewithtropical affinitywhile correcting for phylogenetic autocorrelation, aphylogeneticANOVAwasperformedonthevariablesdescribingthefour syndromes (first principal component of PCA, see section3),using tropical affinity asa fixed, two-level factor,with the functionaov.phyloimplementedintheRpackagegeiger(Harmon,Weir,Brock,Glor,&Challenger,2008).
3 | RESULTS
3.1 | Phylogeny and representativeness of species diversity
Asexpected, the topologyof the time-calibratedphylogeny is con-gruentwiththatobtainedbyZucconetal.(2012).Alsothetopologyof the treegeneratedusing thesupermatrix,which includes169of204(82%)species,islargelycongruentandrecoversthesamemajorclades.Minordifferencesinvolveafewnodeswithlowornosupportandthebranchingorderofafewclades.Thecomparisonofthetime-calibratedandsupermatrix-basedtreesconfirmsthatthe81speciesinthetime-calibratedtreehavebeensampledacrosstheentirefamily,thatallmajorlineagesarerepresentedinthereduceddatasetandthatthespeciesretainedinthesubsequentanalysisareafairrepresenta-tionofthefamilydiversityanddisparity.Thisresultisalogicalconse-quenceofthetaxachoiceoperatedbyZucconetal.(2012),whichwas
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drivenbytaxonomicincentivewithouttakingintoaccountecologicalorlifehistorytraits.
3.2 | Construction of proxies for syndromes
3.2.1 | Ecological specialization
ThePCAbi-plotforecologicalspecializationshowsthatallindicatorsof specialization (“foraging height specialization,” “food specializa-tion,”“habitatspecialization,”“nestheightspecialization,”“altitudinalspecialization”)arepositivelycorrelatedwiththefirstprincipalcom-ponentPC1(explaining20%ofthetotalvariance)whileindicatorsofgeneralism (tolerance), to the exception of “drought tolerance,” arenegativelycorrelatedwithit(Figure1a,Table1).Thesecondprincipalcomponent(PC2,explaining19%ofthetotalvariance)opposes“coldtolerance” to “altitudinal specialization”andcanbe interpretedasa
specific indexofaltitudinalspecialization, fromspeciesrestrictedtolowlands(lowlandspecialists)tospecieswithalargealtitudinalrange(altitudinal generalists). We selected PC1 as the synthetic variablesummarizingbest the informationgivenbyall traitsdescribingeco-logicalspecialization(calledPC1spechereafter).
3.2.2 | r- K gradient
The PC1-PC2 bi-plot for the “r-K-gradient” syndrome (Figure1b)shows that “nesting stage” and “clutch size” (see Appendix S2 fordefinitions)displaythehighestcorrelationvaluewithPC1,whichex-plains36%of the total variation (rs≈0.8, Table1).All indicators ofK-selection (“nesting stage length,” “incubation length,” “number ofbroodsperseason”)butone(“lifeduration”)arepositivelycorrelatedwithPC1,whileindicatorsofr-selection(“clutchsize”and“metabolicrateperunitbodymass”)arenegativelycorrelatedwithit.PC2,which
F IGURE 1 ProjectionintheplaneofthefirsttwoprincipalcomponentsoffourPCAsofthetraitvariablesdescribing(a)ecologicalspecialization,(b)r-Kgradient,(c)sexualselection,(d)social/dispersalbehavior
Shy
Foraging height specialization
Nest height specialization
Food specialization
Altitudinal specialization
Habitat specialization
Drought tolerance
Cold tolerance
Disturbance tolerance
–1.0
–0.8
–0.6
–0.4
–0.2
0.0
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0.8
1.0
–1.0 –0.8 –0.6 –0.4 –0.2 0.0 0.2 0.4 0.6 0.8 1.0
PC2
(19%
)
PC1 (20%)
Clutch size
Nesting stage
Incubation
Breeding season
Broods per season
Life duration
Metabolic rate per unit body mass
–1.0
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–1.0 –0.8 –0.6 –0.4 –0.2 0.0 0.2 0.4 0.6 0.8 1.0PC1 (36%)
PC2
(23%
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Juvenile plumage distinctness
Female plumage drabness
Duration of juvenile plumage
Monogamy
Nest outer diameter
Nest building by males
Incubation by males
Feeding of youngs by males
Size Weight
Bill relative length
Wing relative length
Tail relative length
Tarsus relative length
% melanin
% carotenoid
Rump dichromatism
Head dichromatism
Breast dichromatism
Male plumage brightness
Female plumage brightness
Sexual dimorphism present
Number of notes
Song length
Frequency range
Song mimicry
–1.0
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PC1 (28%)
PC2
(13%
)
Nests dispersed
Breeding dispersion
Breeding dispersion plasticity
Territorial
Gregariousness
Gregariousness plasticity
Mixed partiesMigration
Migration plasticity
–1.0
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PC1 (36%)
PC2
(15%
)
(a) (b)
(c) (d)
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explains 23% of the total variation, ismore trait specific, opposing“metabolicrateperunitweight”to“lifeduration,”displayingthetrivialfact that specieswithhighmetabolic ratehave low lifeduration. Itshouldbenoted that the twovariableswhich arehighly correlatedwithPC2werepoorlydocumented (foronly38%and28%of spe-cies,respectively,seeAppendixS3)comparedtotheothervariablesdescribingther-Kgradient(68%to96%).WethusselectedPC1asasyntheticdescriptorforther-K-gradient,whichwillbefurthercalledPC1rK.
3.2.3 | Sexual selection
InthePC1-PC2bi-plot(Figure1c),thevariables“rumpdichromatism,”“%carotenoid,”and“nestouterdiameter”exhibitthehighestcorrela-tionvalue (rs≈0.8)withPC1 (explaining28%of thetotalvariance).All variables featuring sexdimorphism (including “%carotenoid”) aswell as those related to size (“size,” “weight,” “nest diameter”) arepositivelycorrelatedwithPC1whilevariablesfeaturingtheabsenceorweaknessofsexdimorphism (“femaleplumagebrightness,” “nestbuildingbymales”), including “%melanin,”arenegativelycorrelatedwithit(Table1),suggestingthatPC1canbeusedasaproxyforsexual(Fisherian)selection.However,itmustbenotedthatvariablesmeas-uringtheelaborationofmalesong(“songlength,”“frequencyrange,”“number of notes”) are negatively correlated with PC1, suggestingthat this component opposes two bodies of sexual-selected traits,rather than sexual versus natural selection, as previously thought(Ponge,2013). Itmustalsobenotedthatamongvariablesfeaturingtheshapeofthebody,“wingrelativelength”and“tailrelativelength”(onthenegativeside)areopposedto“tarsusrelativelength”and“billrelativelength”(onthepositiveside)alongthisaxis,suggestingthatthedevelopmentofappendagesusedforflight(wing,tail)isopposedtothoseusedforothermechanical functions (bill, tarsus)alongthisgradientofsexualdimorphism.
Thesignificanceofthiscomplexfactor,whichwewillprovisionallyreferto“sexualdimorphism”ratherthanto“sexualselection,”willbedevelopedinsection4.
Thesecondprincipalcomponent,explainingonly13%ofthetotalvariation,opposes “size” and “weight” tovariablesdescribing sexualdimorphism(allwithpositivescoresalongPC1),indicatingthatamongsexually dimorphic species smaller species exhibit a lowest level ofsexualdifferentiation.ThissubsidiaryPC2componentrepresentedaweakproportionoftraitvariationlinkedtosexualselectionandisnotusedinthefollowinganalyses.
3.2.4 | Dispersal/social behavior
PC1explains36%ofthetotalvariation(Figure1d).Thisfirstprinci-palcomponentishighlycorrelatedwith“breedingdispersion”onthepositive side and “gregariousness” and “breeding dispersion plastic-ity”onthenegativeside(rs≈±0.8,Table1).Indicatorsofterritoriality(“territorial,”“nestsdispersed,”“breedingdispersion”)exhibitpositivescores,inoppositionto“migration,”“gregariousness”andtwoindica-tors of plasticity on thenegative side. PC1 represents a behavioral
gradientfromresident/territorial/solitaryspeciestodispersive/poorlyterritorial/gregariousspecies.PC2(explainingonly15%oftotalvaria-tion)wastraitspecific,opposing“gregariousplasticity”to“gregarious-ness.”PC1wasselectedasthesyntheticvariablebestdescribingthedispersal/socialbehavioralsyndrome,hereaftercalledPC1beh.
3.3 | Ancestrality and evolution of syndromes (H1)
PC1specwasusedtosplitthe81speciesinto33“specialists”and48“generalists”(Fig.S1).Thetransitionratefromgeneralismtowardspe-cialismis0.087,and0.097inthereversedirection.Theancestralstateofecologicalspecializationisthereforeuncertain(Figure2).However,themostlikelyancestralstateforclade1(Fringillinae),themostbasalclade,andforthecoregroup(Carduelinae)isgeneralism,withaprob-abilityof0.82and0.66,respectively,asshownbypiecharts(Figure2).Uncertaintyattherootofthephylogenetictreeismainlyduetoclade2(Euphoninae)whichiscurrentlycomposedofspecialists.Withinthecoregroup(Carduelinae)specialismisnearlyalwaysinaderivedposi-tion,andtheonlycasesofreversalbeingwithinclade5,whilemostextantspeciesinclades3,8,9,10,13,14,and15aregeneralists.
PC1rKwasusedtosplitthe81speciesinto22“K-selected”and59“r-selected”species (Fig.S1).Maximum-likelihoodreconstructionshowedthatr-selectionisthemostlikelyancestralstateforthewholegroup and for most clades,with a transition rate of 0.031 from r-selectiontowardK-selectionandnilinthereversedirection(Figure3).K-selection appears as a derived statewithin Euphoninae tanagers(clade2),Hawaiianhoneycreepers (clade4),Africanserins (clade9),andcrossbills(clade11).
PC1sexwasusedtosplitthe81speciesinto25“sexuallydimorphic”and 56 “sexually monomorphic” species (Fig. S1). Sexual monomor-phismisthemostlikelyancestralstateforthewholegroupandformostclades,withatransitionrateof0.041frommonomorphismtowarddi-morphismandnilinthereversedirection(Figure4).Sexualdimorphismappearsasaderivedstatelimitedtorosefinches(clades5and7),cross-bills(clade11)andisolatedspecieswithinsomeotherclades.
PC1behwasusedtosplitthe81speciesinto31“resident/territo-rial”and50“dispersive/gregarious”species(Fig.S1).Dispersiveness/gregariousness is the most likely ancestral behavioral state, witha transition rate of 0.077 from dispersiveness/gregariousness to-ward residence/territorialityandonly0.033 in the reversedirection(Figure5).SimilarlytoK-selection,residence/territorialityappearsasaderivedstateinEuphoninaetanagers(clade2),Hawaiianhoneycreep-ers (clade4),andAfricanserins (clade9),butnot incrossbills (clade11).Derivationtowardresidence/territorialityisalsoapparentwithinrosefinchesbelongingtoclade5.
3.4 | Correlated evolution of syndromes (H2)
3.4.1 | Modeling and graphical study of the correlated evolution of syndromes
Wemodeledcorrelatedtransitionsbetweenstates(ancestralvs.de-rived) incouplesofsyndromes(Table2).Severalsyndromestendto
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F IGURE 2 Reconstructionbymaximum-likelihoodinferenceoftheancestralstateoftheecologicalspecializationsyndrome,usingthedistributionofspeciesintwogroups(seeFig.S1a).Generalism(stateA)isingraywhilespecialism(stateB)isinblack.Transitionratesfromonegrouptotheotheratthebaseofthephylogenetictreeareindicatedwitharrowsofproportionalthickness.Ateachnodeofthephylogenetictree,apiechartindicatestheconfidencegiventospecialismorgeneralismastheancestralstate.TransitionratesCladenumbersaccordingtoZucconetal.(2012)areindicatedinacolumnontherightsideofthefigure.Amolecularclockisrepresentedatthebottomofthefigure.Geographicdistributionandtropicalaffinityareindicatedforeachspecies(seeincludedlegendforthesignificanceofcodes)
TABLE 1 Listofvariablesselectedforthedescriptionoffoursyndromes,withtheirloadings(=Spearman’srankcorrelationcoefficients)alongthefirstPCAcomponent(oneseparateanalysispersyndrome)
Ecological specialization syndrome PC1spec r- K gradient syndrome PC1rK
Disturbancetolerance −0.39 Clutchsize −0.76
Coldtolerance −0.17 Metabolicrateperunitbodymass −0.31
Shy 0.03 Lifeduration −0.24
Droughttolerance 0.22 Broodsperseason 0.41
Altitudinalspecialization 0.30 Incubation 0.68
Nestheightspecialization 0.48 Breedingseason 0.70
Foodspecialization 0.55 Nestingstage 0.81
Habitatspecialization 0.63
Foragingheightspecialization 0.74
Sexual dimorphism syndrome PC1sex Dispersal/social behavior syndrome PC1beh
Wingrelativelength −0.63 Gregariousness −0.80
Songlength −0.62 Breedingdispersionplasticity −0.75
Femaleplumagebrightness −0.60 Migrationplasticity −0.69
Frequencyrange −0.56 Migration −0.57
%melanin −0.45 Mixedparties −0.23
Tailrelativelength −0.41 Gregariousnessplasticity 0.26
Numberofnotes −0.36 Territorial 0.40
Nestbuildingbymales −0.32 Nestsdispersed 0.64
Juvenileplumagedistinctness −0.27 Breedingdispersion 0.76
Monogamy −0.27
Songmimicry −0.23
Feedingofyoungsbymales −0.06
Incubationbymales 0.26
Billrelativelength 0.27
Maleplumagebrightness 0.28
Tarsusrelativelength 0.32
Femaleplumagedrabness 0.53
Weight 0.58
Sexualdimorphismpresent 0.59
Size 0.62
Durationofjuvenileplumage 0.71
Headdichromatism 0.72
Breastdichromatism 0.75
Nestouterdiameter 0.78
%carotenoid 0.79
Rumpdichromatism 0.81
| 9941PONGE Et al.
Passer luteusPasser montanusPetronia petroniaMontifringilla ruficollisMotacilla albaAnthus trivialisPlectrophenax nivalisAmmodramus humeralisParula pitiayumiLeistes superciliarisFringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospizasipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni Agraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti Leucosticte tephrocotis NAMLeucosticte arctoa Haemorhous mexicanus NAMHaemorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Leistes superciliaris = Outgroup species
Acanthis hornemanni = Generalist species
Loxia pytyopsittacus = Specialist species
= In the tropics
= Out of the tropics
PAL pal = Palearctic distribution (lower case = minor)
ORI ori = Oriental distribution
ARA ara = Arabian distribution
AFR afr = African distribution
NAM nam = North-Central American distribution
SAM sam = South American distribution
HAW = Hawaiian distribution
Fringillidae
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
15 12.5 10 7.5 5 2.5 0 Ma
State A State B
0.087
0.097
9942 | PONGE Et al.
F IGURE 3 Reconstructionbymaximum-likelihoodinferenceoftheancestralstateofther-K-gradientsyndrome,usingthedistributionofspeciesintwogroups(seeFig.S1b).r-selection(stateA)isingraywhileK-selection(stateB)isinblack.Ateachnodeofthephylogenetictree,apiechartindicatestheconfidencegiventoK-selectionorr-selectionastheancestralstate.OtherwiseasforFigure2
Passer luteusPasser montanusPetronia petroniaMontifringilla ruficollisMotacilla albaAnthus trivialisPlectrophenax nivalisAmmodramus humeralisParula pitiayumiLeistes superciliarisFringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospizasipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni PALAgraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti PALLeucosticte tephrocotis NAMLeucosticte arctoa PALHaemorhous mexicanus NAMHaemorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Leistes superciliaris = Outgroup species
Acanthis hornemanni = r-selected species
Loxia pytyopsittacus = K-selected species
= In the tropics
= Out of the tropics
PAL pal = Palearctic distribution (lower case = minor)
ORI ori = Oriental distribution
ARA ara = Arabian distribution
AFR afr = African distribution
NAM nam = North-Central American distribution
SAM sam = South American distribution
HAW = Hawaiian distribution
Fringillidae
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
15 12.5 10 7.5 5 2.5 0 Ma
State A State B
0.031
| 9943PONGE Et al.
F IGURE 4 Reconstructionbymaximum-likelihoodinferenceoftheancestralstateofthesexualdimorphismsyndrome,usingthedistributionofspeciesintwogroups(seeFig.S1c).Sexualmonomorphism(stateA)isingraywhilesexualdimorphism(stateB)isinblack.Ateachnodeofthephylogenetictree,apiechartindicatestheconfidencegiventosexualmonomorphismordimorphismastheancestralstate.OtherwiseasforFigure2
Passer luteusPasser montanusPetronia petroniaMontifringilla ruficollisMotacilla albaAnthus trivialisPlectrophenax nivalisAmmodramus humeralisParula pitiayumiLeistes superciliarisFringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospizasipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni PALAgraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti PALLeucosticte tephrocotis NAMLeucosticte arctoa PALHaemorhous mexicanus NAMHaemorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Leistes superciliaris = Outgroup species
Acanthis hornemanni = Sexual-monomorphic species
Loxia pytyopsittacus = Sexual-dimorphic species
= In the tropics
= Out of the tropics
PAL pal = Palearctic distribution (lower case = minor)
ORI ori = Oriental distribution
ARA ara = Arabian distribution
AFR afr = African distribution
NAM nam = North-Central American distribution
SAM sam = South American distribution
HAW = Hawaiian distribution
Fringillidae
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
15 12.5 10 7.5 5 2.5 0 Ma
State A State B
0.041
9944 | PONGE Et al.
F IGURE 5 Reconstructionbymaximum-likelihoodinferenceoftheancestralstateofthedispersal/socialbehavioralsyndrome,usingthedistributionofspeciesintwogroups(seeFig.S1d).Dispersiveness/gregariousness(stateA)isingraywhileresidence/territoriality(stateB)isinblack.Ateachnodeofthephylogenetictree,apiechartindicatestheconfidencegiventoresidence/territorialityordispersiveness/gregariousnessastheancestralstate.OtherwiseasforFigure2
Passer luteusPasser montanusPetronia petroniaMontifringilla ruficollisMotacilla albaAnthus trivialisPlectrophenax nivalisAmmodramus humeralisParula pitiayumiLeistes superciliarisFringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospizasipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni PALAgraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti PALLeucosticte tephrocotis NAMLeucosticte arctoa PALHaemorhous mexicanus NAMHaemorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Leistes superciliaris = Outgroup species
Acanthis hornemanni = Migrant/gregarious species
Loxia pytyopsittacus = Resident/territorial species
= In the tropics
= Out of the tropics
PAL pal = Palearctic distribution (lower case = minor)
ORI ori = Oriental distribution
ARA ara = Arabian distribution
AFR afr = African distribution
NAM nam = North-Central American distribution
SAM sam = South American distribution
HAW = Hawaiian distribution
Fringillidae
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
15 12.5 10 7.5 5 2.5 0 Ma
State A State B
0.077
0.033
| 9945PONGE Et al.
TABLE 2 Modelingcorrelationsbetweentransitionsfromastate(ancestralAorderivedB)totheoppositestateforfoursyndromes(ecologicalspecialization,r-Kgradient,sexualdimorphism,
dispersal/socialbehavior).Likelihoodratiotest(LRT)wasusedtotestforsignificance.SignificancelevelforLRTp-valuewasfixedto.05.Boldtypesindicatesignificantrelationshipsbetween
transitionstatesofsyndromes.Detailsarethengivenontransitionratesforpairsofsyndromeswheretransitionsbetweencharacterstatesaresignificantlycorrelated
Synd
rom
e 1
Synd
rom
e 2
Like
lihoo
d in
depe
nden
tLi
kelih
ood
depe
nden
tLR
T st
atis
ticLR
T p-
valu
e
Sexualdimorphism
r-Kgradient
−64.798251
−62.977532
3.641438
0.456700628
Sexualdimorphism
Dispersal/socialbehavior
−73.281643
−71.241161
4.080964
0.39
5159
442
Sexu
al d
imor
phis
mEc
olog
ical
spec
ializ
atio
n−8
2.58
8379
−77.
7938
069.
5891
460.
0479
4737
6
r-K
grad
ient
Dis
pers
al/s
ocia
l beh
avio
r−7
9.52
8616
−72.
3098
6314
.437
506
0.00
6022
008
r-Kgradient
Ecologicalspecialization
−88.835352
−84.850098
7.97
0508
0.092664518
Dis
pers
al/s
ocia
l beh
avio
rEc
olog
ical
spec
ializ
atio
n−9
7.31
8748
−83.
4467
9227
.743
912
1.40
558E
-05
Cond
ition
al sy
ndro
me
stat
eD
epen
dent
synd
rom
e tr
ansi
tion
Dep
ende
nt tr
ansi
tion
rate
Sexualselectionandecologicalspecialization
Sexualdimorphism=A
EcologicalspecializationA→B
0.068022
Sexualdimorphism=A
EcologicalspecializationB→A
0.04
9974
Sexualdimorphism=B
EcologicalspecializationA→B
1.616921
Sexualdimorphism=B
EcologicalspecializationB→A
1.47
2791
Ecologicalspecialization=A
SexualdimorphismA→B
0.01
5748
Ecologicalspecialization=A
SexualdimorphismB→A
0a
Ecologicalspecialization=B
SexualdimorphismA→B
0.060825
Ecologicalspecialization=B
SexualdimorphismB→A
0.000164
b
r-Kgradientanddispersal/socialbehavior
r-Kgradient=A
Dispersal/socialbehaviorA→B
0.05
2294
r-Kgradient=A
Dispersal/socialbehaviorB→A
0.169471
r-Kgradient=B
Dispersal/socialbehaviorA→B
0.47
751
r-Kgradient=B
Dispersal/socialbehaviorB→A
0c
Dispersal/socialbehavior=A
r-KgradientA→B
0.04
4915
Dispersal/socialbehavior=A
r-KgradientB→A
0d
Dispersal/socialbehavior=B
r-KgradientA→B
0e
Dispersal/socialbehavior=B
r-KgradientB→A
0.07
2745
Ecologicalspecializationanddispersal/socialbehavior
Ecologicalspecialization=A
Dispersal/socialbehaviorA→D
0.046407
Ecologicalspecialization=A
Dispersal/socialbehaviorD→A
0.083369
Ecologicalspecialization=D
Dispersal/socialbehaviorA→D
0.14
2005
Ecologicalspecialization=D
Dispersal/socialbehaviorD→A
0f
(Continues)
9946 | PONGE Et al.
followcommonpaths,inparticular(1)sexualdimorphismandecologi-calspecialization, (2) r-K-gradientanddispersal/socialbehavior,and(3) ecological specialization and dispersal/social behavior. Reversalfrom derived to ancestral state never or hardly occurs when onememberofthesethreecouplesofsyndromesisinderivedstate(seetransitionratesinTable2).
The correlated evolution of the four syndromeswas then visu-allyaddressedbyreportingonthesamegraphintheformofcoloredtrajectories (Figure6) themaximum-likelihoodpatternsdisplayedbyFigures2–5.Totheexceptionofgeneralism,forwhichuncertaintyre-mains at thebaseof the tree, theancestralityof r-selection, sexualmonomorphism,anddispersiveness/gregariousnessismorelikelythantherespectivealternativestateofeachsyndrome.Althoughthecor-relatedevolutionofmorethantwosyndromescouldnotbemodeledbyourmethod,Figure6showsthatthreesyndromescanfollowthesamepath,althoughall thefoursyndromesnever followacommonpath.Hence,ourformer,simplistichypothesisoftheexistenceoftwooppositestrategies,evolvingfromanancestralstrategyA(generalists,r-selected,sexuallymonomorphic,migratory/gregarious)toaderivedstrategyB(specialists,K-selected,sexuallydimorphic,resident/terri-torial)shouldberefinedbyconsideringthatthesefoursuitesoftraitsdivergedinthecourseofevolution,generatingmorethanonederivedstrategy.
3.4.2 | Multivariate analysis of phylogenetic signaling
A phylogenetic PCA (pPCA) performed on the four syndromes(PC1spec,PC1rK,PC1sex,PC1beh)wasusedforafinerdelineationofgroupsofspeciesthatareassociatedtosyndromeshavingevolvedcorrelatively.Thefoursyndromesexhibiteachasignificantphyloge-netic signal (Abouheif’s test,p<.01). The first three principal com-ponents of pPCA exhibit positive eigenvalues (Table3, Figure 8c),indicatingtheexistenceofaphylogeneticsignaloneachofthem.ThefirstcomponentofpPCAdisplaysaphylogeneticsignalcommontoallfoursyndromes(Figure8a,b),whilesecond(Figure8a)andthirdcom-ponents (Figure8b)partialoutphylogeneticsignalsofsomegroupsofsyndromes.
ThefirstprincipalcomponentpPC1opposesA-strategists(gener-alist,r-selected,sexuallymonomorphic,gregarious/migratoryspecies),toB-strategists (specieswithopposite traitmodalities), asexpectedfrom our Hypothesis H2 (Figure 8a,b). However, the two followingprincipalcomponentspPC2andpPC3showthatstrategyBcouldbedivided into two strategies,whichwe call B1 andB2 (Figure 8a,b).StrategyB1 ischaracterizedbyacombinationofsexualdimorphismandr-selection (Figure8b)whilestrategyB2 ischaracterizedbythecommon occurrence of residence/territoriality (Figure 8a) and K-selection(Figure8b).TheoriginalityofstrategyB1isthatitcombinestraitmodalities of strategyA (r-selection) and strategyB (sexual di-morphism),while strategyB2 is characterized by traitmodalities ofstrategyB,totheexceptionofsexualdimorphism.
Weusedthe3DspaceofthefirstthreeprincipalcomponentsofpPCAtosplitthewholesetofspeciesintothosethreestrategies(A,B1,B2)with thek-meansmethodofvariancepartition (withk=3).
Cond
ition
al sy
ndro
me
stat
eD
epen
dent
synd
rom
e tr
ansi
tion
Dep
ende
nt tr
ansi
tion
rate
Dispersal/socialbehavior=A
EcologicalspecializationA→D
3.81
304
Dispersal/socialbehavior=A
EcologicalspecializationD→A
9.535607
g
Dispersal/socialbehavior=D
EcologicalspecializationA→D
0h
Dispersal/socialbehavior=D
EcologicalspecializationD→A
0h
a Whenecologicalspecialization=A,thensexualdimorphismnevershiftsfromDtoA.
b Whenecologicalspecialization=D,thensexualdimorphismhardlyshiftsfromDtoA.
c Whenr-Kgradient=D,thendispersal/socialbehaviornevershiftsfromDtoA.
d Whendispersal/socialbehavior=A,thenr-KgradientnevershiftsfromDtoA.
e Whendispersal/socialbehavior=D,thenr-KgradientnevershiftsfromAtoD.
f Whenecologicalspecialization=D,thendispersal/socialbehaviornevershiftsfromDtoA.
g Whendispersal/socialbehavior=A,thenecologicalspecializationoftenshiftsfromDtoA.
h Whendispersal/socialbehavior=D,thenecologicalspecializationneithershiftsfromAtoDnorfromDtoA.
TABLE 2 (Conttinued)
| 9947PONGE Et al.
F IGURE 6 Commonrepresentationofpathsfollowedbyecologicalspecialization,r-K-gradient,sexualdimorphism,anddispersal/socialbehavioralongthephylogenetictreeof81fringillidspecies.Colorlinesareforderivedstates,graylinesforancestralstates,theyweredashedincaseofincertitude.Speciesnamesareingray(Astrategy),blackitalics(B1strategy),orblackroman(B2strategy).OtherwiseasforFigure2
Fringillidae
Fringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospiza sipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni PALAgraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti PALLeucosticte tephrocotis NAMLeucosticte arctoa PALHaemorhous mexicanus NAMHeamorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
= Specialist
= K-selected
= Sexually dimorphic
= Resident/territorial
Spinus tristis = State A speciesCrithagra leucopygia = State B1 speciesLoxia leucoptera = State B2 species
= in the tropics= out of the tropics
PAL pal = Palearctic distribution (lower case = minor)ORI ori = Oriental distributionARA ara = Arabian distributionAFR afr = African distributionNAM nam = North-Central American distributionSAM sam = South American distributionHAW = Hawaiian distribution
15 12.5 10 7.5 5 2.5 0 Ma
9948 | PONGE Et al.
ThethreestrategiesareindicatedonFigure6.ThereconstructionofancestraltraitsgivesafullsupporttotheancestralityofstrategyAandtoderivedpositionsforstrategiesB1andB2(Figure7).ThehighesttransitionrateisfromAtowardB1(0.067),followedbyAtowardB2(0.027),whilereversal ratesarenil.TransitionfromB2towardB1 ispossiblebutlessfrequentthantransitionfromAtoeitherstrategyB(transitionrate0.014),whiletransitionfromB1towardB2neveroc-curs.StrategyAisexpressedinclades1,8,10,13–15,partlyinclades3and11.StrategyB1isexpressedinclades5and7,partlyinclades6and11,whiletheB2strategyisexpressedinclades2,4,and9.
3.5 | Association of syndromes with tropical affinity (H3)
We tested whether there was a latitudinal signal (tropical affinity)in the distribution of syndrome states by performing phylogeneticANOVAs. K-selection and residence/territoriality exhibit the samesignificantaffinityfortropicalareas,whilesexualdimorphismexhibitsahigheraffinityfornontropicalareas,andspecialismdoesnotdisplayanysignificantlatitudinalsignal(Table4).
4 | DISCUSSION
4.1 | Ancestral syndromes in Fringillidae
ResultssupportourH1hypothesis:r-selectionanddispersiveness/gre-gariousnessareancestralandtendtoshifttowardderivedattributesinthecourseofevolution.Eventhoughmostspecies/traitsarespreadalongacontinuousr-Kgradient(Jones,1976),ithasbeentheoretically(Blanck,Tedesco,&Lamouroux,2007)andempiricallydemonstrated(Flegr,1997)thatspecieswhosereproductivestrategyliesinthemid-dleofther-Kcontinuumareatdisadvantage,justifyingthedistinctionoftwooppositestrategies.Ourqualitativeapproachshowstwogroupsof r-selected andK-selected species.Comparisons between tropicalandnontropicalbirdspeciesshowedanassociationofK-strategy(ap-proximatedbybasalmetabolic rate)with climatically stableenviron-ments(Wiersma,Muñoz-Garcia,Walker,&Williams,2007),supportingtheoreticalexpectations(Southwood,May,Hassell,&Conway,1974).
Thereconstructionofancestraltraitsforthebehavioralsyndromeshowsthatbehavioralplasticityandgregariousnesshaveabasalpo-sitionwhileratherstandardizedandsolitarybehaviorsareinderivedposition(Figure5),asshownbySimpson,Johnson,andMurphy(2015)inParulidae.Heretoo,thissyndromeisclearlyrelatedtothestabilityoftheenvironment,gregariousnessanddispersalabilitybeingadvan-tageous formotileorganismsfacingenvironmentalhazards (Stevens
etal., 2014).Wemay add that once bursts of speciation appear innovelenvironments,ancestraltraitsassociatedwithmigration(inpar-ticularorientationandmemorizationofgeographicfeatures,togetherwithcollectivebehavior)maydisappearinfavorofsophisticatedsig-nalingtraitsassociatedwithterritorialityifthecolonizedenvironmentturnsouttobemorestablethantheoriginalenvironment,acaseofrelaxedselectionpressure(Wiersma,Nowak,&Williams,2012).
Theancestralreconstructionofthe“sexualdimorphism”syndromeshowsthatagroupofsexuallyselectedtraitsrelatedtomalesongelab-oration (Table1) is inancestralpositionwhileagroupof sexually se-lectedtraitsrelatedtoplumagecolorandbodysizeisinderivedposition(Figure4).Thisisnotinagreementwithouroriginalhypothesisofnat-uralselectionopposedtosexualselection,theformerprocessbeingaresponsetofluctuationsoftheenvironmentwhilethelatterwoulddrivedirectional evolution in stable environments (Møller & Garamszegi,2012).However,ithasbeenshownthatsexualselectionisalsoanadap-tiveresponsetoenvironmentalconstraintsandfluctuations (Badyaev&Ghalambor,1998),andthatsynergisticcombinationsofnaturalandsexualselectionarewidespread(Botero&Rubenstein,2012).Theop-positionbetweenvisual(size,color)andacousticsignals(songdisplay)has been already observed by Badyaev etal. (2002) in Carduelinae.Suchareversalfromonetypeofsexuallyselectedsignaltoanotherisknownasthe“transferhypothesis”(Shutler&Weatherhead,1990).Theobservedcontrastbetweensongelaborationandcolordisplayisparal-leledbyacontrastbetweenmelaninandcarotenepigmentsinplumagecoloration(Table1).Bothmelanin-andcarotene-basedplumagecolorshavebeenshowntopredictsuccessindominanceinteractionsbetweenmalesandinfluencefavorablyfemalechoices(Hill,1990;Tarof,Dunn,&Whittingham,2005)andarehonestsignalsofmalegoodconditionand resistance to parasites (Roulin, 2015; Safran, McGraw, Wilkins,Hubbard,&Marling,2010).However,carotenemustbefound intheenvironmentwhilemelanin isproducedbybirds themselves (Griffith,Parker,&Olson,2006;Roulin,2015).Wehypothesizethatinenviron-mentswherefoodresourcesarescarce,theabilityofmalestofindhigh-qualityresourcesandallocatethisqualitytooffspringisadvantageoustosurvivaland isfavoredbymates (carotene-basedsexualselection).Conversely,inenvironmentswhereresourcesareabundant,atleastinbreedingareas,melanin,whichisnotcontextdependentbutpleiotrop-icallylinkedtobodyconditionandstronglyheritable(Roulin,2015),isfavoredbymates(melanin-basedsexualselection).
The ancestrality of dispersiveness (see above) suggests that an-cestral true finches (Fringillidae)weremonomorphic (melanin-basedconspicuous plumage in both sexes) had elaborated song andwerewell-equipped for flying to remote breeding areaswhere resourcesare seasonally abundant, while dimorphic (carotene-based colored)
PC1 PC2 PC3
Ecologicalspecialization −0.4976956 −0.03918335 0.26095389
r-Kgradient −0.22146655 −0.44248631 0.77233494
Sexualdimorphism −0.80095985 −0.12831694 −0.47739305
Dispersal/socialbehavior −0.248425 0.88668218 0.3278684
Eigenvalue 0.1587 0.0789 0.0642
TABLE 3 Phylogeneticprincipalcomponentsanalysis.Scoresofthefoursyndromesalongthefirstthreeprincipalcomponents.Eigenvaluesaregiveninthelastrow
| 9949PONGE Et al.
F IGURE 7 Reconstructionbymaximum-likelihoodinferenceoftheancestralstateofthethreestrategiesA(green),B1(blue),andB2(red),usingthedistributionofspeciesinthreegroupsaccordingtok-meansclusteringbasedonthefirstthreeprincipalcomponentsofphylogeneticPCA.Ateachnodeofthephylogenetictree,apiechartindicatestheconfidencegiventoresidence/territorialityordispersiveness/gregariousnessastheancestralstate.OtherwiseasforFigure2
Passer luteusPasser montanusPetronia petroniaMontifringilla ruficollisMotacilla albaAnthus trivialisPlectrophenax nivalisAmmodramus humeralisParula pitiayumiLeistes superciliarisFringillacoelebs PALFringillamontifringilla PALChlorophonia cyanea SAMEuphonia musica NAM SAMEuphonia chlorotica SAMEuphonia cayennensis SAMEuphonia xanthogaster SAMEuphonia minuta NAM SAMEuphonia laniirostris NAM SAMEuphonia violacea SAMMycerobas carnipes PALEophona migratoria PAL namHesperiphona vespertina NAMCoccothraustes coccothraustes PALParoreomyza montana HAWLoxioides bailleui HAWChlorodrepanis virens HAWErythrina erythrina PAL ORIHaematospizasipahi PAL oriCarpodacus synoicus PAL araCarpodacus sibiricus PALCarpodacus puniceus PALCarpodacus roseus PALCarpodacus thura PALCarpodacus rubicilloides PALCarpodacus rubicilla PALCarpodacus pulcherrimus PALCarpodacus rodochroa PALCarpodacus rhodochlamys PALPinicola enucleator PAL NAMProcarduelis nipalensis PAL ORIPyrrhula pyrrhula PALPyrrhula erythaca PAL ORIRhodopechys sanguineus PALBucanetes githagineus PAL ARA AFREremopsaltria mongolica PALCallacanthis burtoni PALAgraphospiza rubescens PALLeucosticte nemoricola PALLeucosticte brandti PALLeucosticte tephrocotis NAMLeucosticte arctoa PALHaemorhous mexicanus NAMHaemorhous purpureus NAMRhodospiza obsoleta PAL ARAChloris chloris PALChloris sinica PAL oriChloris monguilloti ORIChloris spinoides PAL oriChloris ambigua PAL ORISpinus olivaceus PALCrithagra striolata AFRCrithagra burtoni AFRCrithagra mennelli AFRCrithagra sulphurata AFRCrithagra rufobrunnea AFRCrithagra citrinelloides AFRCrithagra mozambica AFRCrithagra leucopygia AFRLinaria cannabina PALLinaria flavirostris PALAcanthis flammea PAL NAMAcanthis hornemanni PAL NAMLoxia leucoptera PAL NAMLoxia pytyopsittacus PALLoxia curvirostra PAL ORI NAM samCarduelis carduelis PALCarduelis citrinella PALSerinus canicollis AFRSerinus syriacus PALSerinus pusillus PALSerinus serinus PALSerinus canaria PALSpinus psaltria NAM SAMSpinus tristis NAMSpinus spinus PAL oriSpinus pinus NAMSpinus barbatus SAMSpinus cucullatus SAMSpinus magellanicus SAMSpinus atratus SAM
Leistes superciliaris = Outgroup species
Spinus tristis = State A species
Loxia leucoptera = State B1 species
Crithagra leucopygia = State B2 species
= In the tropics
= Out of the tropics
PAL pal = Palearctic distribution (lower case = minor)
ORI ori = Oriental distribution
ARA ara = Arabian distribution
AFR afr = African distribution
NAM nam = North-Central American distribution
SAM sam = South American distribution
HAW = Hawaiian distribution
Fringillidae
Fringillinae
Euphoniinae
Carduelinae
1
2
3
4
5
6
7
8
9
10
11
13
14
15
15 12.5 10 7.5 5 2.5 0 Ma
Strategy A
Strategy B1 Strategy B2
0.014
9950 | PONGE Et al.
resident birds are better equipped for foraging in areas where re-sources are scarcely distributed. The ancestrality of monochroma-tism(malesandfemalesbothharboringabrightcoloration)hasbeendemonstrated in other bird groups (Friedman, Hofmann, Kondo, &Omland,2009;Simpsonetal.,2015).
OurhypothesisofgeneralismasancestralintheFringillidaecannotberejected,becauseoftwoarguments.First,generalismisanancestralstateinCarduelinae,thecoregroupand,second,thetwospeciesofthemostbasal subfamily, theFringillinae,whichare included inourstudy(F. coelebsandF. montifringilla),areclearlygeneralists. Itshouldalsobenotedthatreversalfromspecialismtogeneralismisobservedinclade5only (Figure2).Therefore,despiteuncertaintyofancestral reconstruc-tion,specialismisaderivedstateinallcladesbutclade5.Animportantpointisthatgeneralismisstillthecommoneststateinthecrowngroup(clades7to15,Figure2),thatis,incladesmostremotefromthecommonancestorandthusresultingfromahighnumberofspeciationevents.
Theancestralityofgeneralismhasbeendemonstratedinavarietyofmonophyletic groups, amongplants (Schneeweiss, 2007;Tripp&Manos,2008)andanimals(Hwang&Weirauch,2012;Kelley&Farrell,1998;Loiseauetal.,2012;Prinzing,D’Haese,Pavoine,&Ponge,2014;Yotoko&Elisei,2006),birdsincluded(Brumfieldetal.,2007;Jønsson,Fabre,Ricklefs,&Fjeldså,2011),whilefewerstudiesconcludetotheancestralityofspecialism(Sedivy,Praz,Müller,Widmer,&Dorn,2008;Stireman,2005).Despite repeatedassessmentofphylogenetic con-servatism of niche requirements (Brumfield etal., 2007; Peterson,Soberón,&Sánchez-Cordero,1999;Prinzing,Durka,Klotz,&Brandl,2001;Prinzingetal.,2014;Wiens&Graham,2005),confirmedinthepresent study, ithasevenbeen shown thathabitat specialization isalabileecologicaltraitthatmaychangeintheshort-termwithinthesame species (Barnagaud, Devictor, Jiguet, & Archaux, 2011). Thismightexplainwhyancestralattributesofecologicalspecializationarelessclear-cutthanforr-K,sexualselection,andbehavioralsyndromes.
4.2 | The correlated evolution of syndromes in Fringillidae
Eventhoughwedonotrecordacorrelatedevolutionofallfoursyn-dromes,acommonphylogeneticsignalisdetected(Table3)andthreesyndromesexhibitacorrelatedevolutionalongthephylogenetictree
(r-K-gradient,ecologicalspecialization,anddispersal/socialbehavior,Table3,Figure6).Sexualdimorphismappearstohaveevolvedinas-sociationwithancestraltraitmodalitiesofthethreeothersyndromes(Figures6and8)andisnotassociatedwithK-selectionandresidence/territoriality (with theexceptionof thegenusLoxiawithin clade11,associatedwithK-selection,seeFigure3).Thisfeatureexplainswhyacommonevolutionofthefoursyndromeswasnotdetected.However,r-selected traits, sexualmonomorphism, anddispersiveness/gregari-ousness areall present in ancient lineages in thephylogenetic tree,supportingatleastpartiallyourhypothesisH2thatsyndromesevolvedcorrelativelyalongthephylogenetictreeofFringillidae.
Our results point to the existence of a common ancestor toFringillidaewithallfeaturesoftheAstrategy(generalism,r-selection,monochromatism with elaborated song, dispersiveness/gregarious-ness),withafurtherevolutionofagroupofcladeswheresexualdi-morphismisprominentwhileotherfeaturesoftheAstrategyarekept(strategyB1),andanothergroupwheremostfeaturesoftheBstrategyevolvedtotheexceptionofsexualdimorphism(strategyB2;Figure7).
4.3 | Geographical distribution and past history of the Fringillidae
Wemaywonderwhethertheobserveddiscrepancybetweenalineagewithsexuallyselecteddimorphism(B1)andanotherwithK-selected,specialist, and resident/territorial traits (B2) could be explained bygeographical affinities of the species, and the way different envi-ronmentswerecolonizedinthecourseoftheevolutionofthisnowworldwidebirdfamily.Ifweexaminetherelationshipbetweentropi-calaffinityandthebalancebetweenancestralandderivedstatesofourfoursyndromes(Table4),itappearsthatmosttropicalspeciesareK-selectedandresidentterritorialwhilemostnontropicalspeciesaredimorphic sexually, and ecological specialization is undifferentiated.Thisresultsupportsonlypartlyourthirdhypothesis(H3)thatderivedattributesareassociatedwithtropicalaffinity,suggestingthattheB2type lives (andprobablyevolved)mainly in tropicalareas,while theB1branchislocated(andprobablyevolved)mainlyoutofthetropics.
Theexistenceofasexuallydimorphicbranchlivingoutofthetropicsissupportedbystudiesonotherbird families (Bailey,1978;Friedmanetal.,2009),whilePrice,Lanyon,andOmland(2009)pointedonsing-ingbybothsexesas the tropical ancestral state inNewWorldblack-birds.Speciesweclassifiedinthesexuallydimorphicgroup(Fig.S1c)aremostlyadaptedtolifeinharshenvironments.Anextraordinaryvarietyoftruerosefinches(clade5)arelivingintheHimalayas,whicharethoughtto be a source of species radiation (Tietze etal., 2013).Within clade6, the trumpeter finchBucanetes githagineus and theMongolian finchEremopsaltria mongolicaliveindesertsorsemi-deserts,andtheBlanford’srosefinchAgraphospiza rubescenslivesintheHimalayas.Otherspeciesofthisgrouphaveacircumpolardistributionandliveinconiferousforests(thewhite-wingedcrossbillLoxia leucoptera, theredcrossbillLoxia cur-virostra).However,mountain finches (Leucosticte) live inAsian tundrasand highmountains and display no or onlyweak sexual dimorphism,thustoleranceofharshhabitatsdoesnotnecessarilyentailsexualdimor-phism.Contrarytoerroneousideasresultingfromtheordinaryconfusion
TABLE 4 Relationshipbetweensyndromegroupsandtropicalaffinity,testedbyphylogeneticANOVA(ANOVAcorrectedforphylogeneticautocorrelation)
Tropical affinity F- value Probability
Generalistvs.specialist 0.41vs.0.53 0.17 0.81NS
r-Selectedvs.K-selected
0.35vs.0.77 13.25 0.025*
Sexualmonomorphismvs.sexualdimorphism
0.56vs.0.23 12.52 0.026*
Dispersive/gregariousvs.resident/territorial
0.33vs.0.68 12.02 0.032*
NS=notsignificantat0.05level;*p<.05.
| 9951PONGE Et al.
betweenstressanddisturbance(Borics,Várbiró,&Padisák,2013),suchharshhabitatsarehighlypredictable (Greenslade,1983),allowingsea-sonalshort-distance (altitudinal)or long-distance (latitudinal)migrationto cope with foraging and breeding bird requirements. According toPonge(2013)cyclic,seasonalprocessestowhichorganismsareadaptedallowsanticipation,akeyadaptivetraitofstrategyB.
The existenceofK-selected, resident/territorial (also specialist?)B2-strategistslivinginthetropicsisattestedbymanystudiesonbirds(Jetz,Freckleton,&MvKechnie,2008;Soletal.,2010;Wiersmaetal.,2007,2012).WemaythusconsiderthatstrategyB2isassociatedwithstable benign environments, better exemplified near the Equator intropicalrainforests.
5 | CONCLUSIONS
Our results provide strong support to strategy A (r-selection, sexualmonomorphism,migratory/gregarious)asancestralinthefringillidfam-ily.However,ourformerideaoftwooppositestrategiespreviouslycalled“barbarians” (ancestral) and “civilized” (derived) by Ponge (2013), andnowcalledAandB,respectively,mustberefined.StrategyB,associatedwithpredictabilityoftheenvironment,shouldbesubdividedinB1(sexu-allydimorphic,r-selected,migratory/gregarious),associatedwithharshhabitats (mountainandborealhabitats),mostlyoutofthetropics,andB2 (sexuallymonomorphic, K-selected, resident/territorial), associated
withmostbenignhabitats,mostlyinlowlandtropics.BothhabitatsofB-organismsarepredictable,althoughinB1thehighseasonalityforcesspe-ciestomigrateseasonally(eitheraltitudinalorlatitudinalmigration)whileinB2theancestralmigratorybehaviorhasbeenlost,beingunnecessary.
ACKNOWLEDGMENTS
WearegratefultoPeterClement,ClaireDoutrelant,andDorisGomezforconstructivecommentsonafirstdraftofthemanuscript.
CONFLICT OF INTEREST
Nonedeclared.
AUTHORS CONTRIBUTION
Jean-FrançoisPongeperformedmostpartoftheredaction,partofthecalculations(constructionofthesyntheticvariablesasproxiesfortraitsyndromes),madegraphicalrepresentationsoftheresults,andcollectedthe original data in published literature. Dario Zuccon performed thephylogenyandcontributedtotheredaction.MarianneEliasperformedthereconstructionofancestraltraitsyndromesandsomeothercalcula-tions,andcontributedtotheredaction.SandrinePavoineperformedthephylogeneticPCAandsomeothercalculationsandcontributedtotheredaction.Pierre-YvesHenrycontributedtotheredactionandtofruitful
F IGURE 8 Projectionintheplaneofthefirstandsecond(a),andfirstandthird,(b)principalcomponentsofphylogeneticPCAofthesyntheticvariables(seetextfordetails)describingthefourstudiedsyndromes.Eigenvaluesarediagrammaticallyrepresented(c)
Specialism
K-selec�on
Sexual dimorphism
Residence territoriality Strategy A
Strategy B1
Strategy B2
pPC1pP
C2
(a)
Specialism
K-selec�on
Sexual dimorphism
Residence territoriality
Strategy A
Strategy B1
Strategy B2
pPC1
pPC3
(b)
0
0.05
0.1
0.15
0.2
pPC1 pPC2 pPC3 pPC4
(c)
9952 | PONGE Et al.
discussionsaboutmethodsandconcepts.MarcThéryandÉricGuilbertcontributedtotheredactionandtofruitfuldiscussions.
ORCID
Jean-François Ponge http://orcid.org/0000-0001-6504-5267
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SUPPORTING INFORMATION
Additional Supporting Informationmay be found online in the sup-portinginformationtabforthisarticle.
How to cite this article:PongeJ-F,ZucconD,EliasM,etal.Ancestralityandevolutionoftraitsyndromesinfinches(Fringillidae).Ecol Evol. 2017;7:9935–9953. https://doi.org/10.1002/ece3.3420
Figure S1. Scores (loadings) of 81 fringillid species along the first axis of the four PCAs featuring ecological specialization (a), r-K gradient (b), sexual selection (c) and dispersal/social behaviour (d).
Spinus magellanicusErythrina erythrina
Carpodacus roseusAcanthis flammeaCrithagra striolata
Fringilla montifringillaHaemorhous purpureus
Pyrrhula pyrrhulaFringilla coelebs
Chloris sinicaHaematospiza sipahi
Spinus psaltriaPinicola enucleator
Spinus tristisCarduelis carduelis
Spinus pinusSpinus barbatusChloris spinoides
(a)Fringilla montifringilla
Acanthis flammeaCarduelis carduelis
Acanthis hornemanniErythrina erythrina
Leucosticte arctoaCarpodacus rubicilloides
Carpodacus rodochroaEophona migratoria
Euphonia cayennensisFringilla coelebs
Agraphospiza rubescensSpinus tristis
Haematospiza sipahiCarpodacus thuraLinaria flavirostrisPyrrhula pyrrhula
Bucanetes githagineus
(b)
Chloris spinoidesChloris chlorisSerinus pusillus
Carpodacus rodochroaCrithagra sulphurata
Rhodospiza obsoletaCarduelis citrinella
Crithagra rufobrunneaCrithagra burtoni
Carpodacus rubicillaCrithagra mozambica
Crithagra mennelliCarpodacus rhodochlamys
Eophona migratoriaChlors ambigua
Serinus serinusSerinus canaria
Coccothraustes coccothraustesSpinus olivaceus
Linaria flavirostrisAcanthis hornemanni
Spinus spinusLinaria cannabina
Hesperiphona vespertinaSerinus canicollis
Bucanetes githagineusCoccothraustes coccothraustes
Linaria cannabinaCarpodacus puniceus
Chloris chlorisCarpodacus sibiricus
Rhodopechys sanguineusCarpodacus pulcherrimus
Chloris sinicaCarpodacus rhodochlamys
Leucosticte nemoricolaSpinus spinus
Euphonia xanthogasterSpinus atratus
Haemorhous purpureusSpinus psaltria
Rhodospiza obsoletaEremopsaltria mongolica
Carpodacus synoicusSerinus pusillus
Spinus cucullatusPinicola enucleator
Chloris spinoidesSerinus syriacus
Leucosticte brandtiSerinus canicollisProcarduelis nipalensisLoxia curvirostraHaemorhous mexicanusMycerobas carnipesChloris monguillotiLeucosticte nemoricola
Spinus atratusCrithagra citrinelloides
Carpodacus rubicilloidesRhodopechys sanguineusCarpodacus pulcherrimusCarpodacus puniceusSpinus cucullatusPyrrhula erythacaChlorodrepanis virensEuphonia laniirostrisCarpodacus thura
Bucanetes githagineusCarpodacus sibiricus
Callacanthis burtoniSerinus syriacus
Loxia leucopteraCarpodacus synoicus
Leucosticte brandtiChloris monguilloti
Hesperiphona vespertinaEuphonia musica
Carpodacus rubicillaSerinus serinus
Carpodacus roseusSpinus pinusChloris ambiguaLeucosticte tephrocotisProcarduelis nipalensis
Carduelis citrinellaEuphonia chloroticaCallacanthis burtoniHaemorhous mexicanusSpinus barbatusSerinus canicollis
Spinus olivaceusSerinus canaria
Crithagra mennelliEuphonia violacea
Crithagra striolataCrithagra leucopygiaCrithagra sulphurataCarpodacus synoicus
Euphonia xanthogasterEuphonia chlorotica
Leucosticte brandtiCrithagra leucopygiaEuphonia musica
Euphonia violaceaEremopsaltria mongolica
Loxia pytyopsittacusLeucosticte tephrocotisAgraphospiza rubescensEuphonia cayennensisLeucosticte arctoa
Chlorophonia cyaneaParoreomyza montana
Euphonia minutaLoxioides bailleui
-6 -4 -2 0 2 4 6
First component of PCA (generalists → specialists)
Crithagra sulphurataCrithagra citrinelloides
Pyrrhula erythacaSpinus magellanicusChlorodrepanis virens
Mycerobas carnipesEuphonia laniirostrisEuphonia minuta
Loxia leucopteraLoxia pytyopsittacusLoxia curvirostraParoreomyza montanaCrithagra mozambica
Crithagra rufobrunneaChlorophonia cyanea
Crithagra burtoniLoxioides bailleui
-6 -4 -2 0 2 4 6 8
First component of PCA (r-selected → K-selected)
Carduelis carduelisCarduelis carduelisCrithagra leucopygia
Serinus pusillusSpinus pinus
Paroreomyza montanaCrithagra striolata
Serinus citrinellaLeucosticte nemoricola
Euphonia laniirostrisCrithagra rufobrunnea
Crithagra mennelliEuphonia minuta
Crithagra mozambicaEuphonia violacea
Serinus serinusChlorodrepanis virens
Spinus atratusLeucosticte arctoa
Loxioides bailleuiCrithagra citrinelloides
Serinus syriacusSerinus canicollis
Serinus canariaChloris ambigua
Euphonia musica
(c)Spinus pinus
Linaria cannabinaEremopsaltria mongolica
Linaria flavirostrisSpinus tristis
Leucosticte arctoaChloris chloris
Acanthis hornemanniSpinus spinus
Loxia pytyopsittacusLoxia leucoptera
Leucosticte brandtiHaemorhous mexicanus
Loxia curvirostraSerinus canaria
Bucanetes githagineusAcanthis flammea
Spinus barbatusCarduelis carduelis
Rhodopechys sanguineusCoccothraustes coccothraustes
Rhodospiza obsoletaCarduelis citrinella
Chloris spinoides
(d)
Euphonia musicaSpinus psaltria
Rhodospiza obsoletaChloris sinica
Crithagra burtoniAcanthis hornemanni
Chloris monguillotiChloris spinoides
Leucosticte brandtiSpinus magellanicus
Euphonia cayennensisLinaria flavirostrisSpinus cucullatus
Chlorophonia cyaneaSpinus spinus
Euphonia chloroticaSpinus barbatus
Procardualis nipalensisSpinus olivaceus
Fringilla coelebsCrithagra sulphurata
Chloris chlorisFringilla montifringilla
Spinus tristis
Chloris spinoidesLeucosticte nemoricola
Erythrina erythrinaFringilla montifringilla
Spinus psaltriaSerinus syriacus
Carpodacus roseusSerinus pusillus
Serinus serinusSerinus canicollis
Leucosticte tephrocotisChloris sinica
Carpodacus rubicillaChloris ambigua
Spinus magellanicusHaemorhous purpureus
Fringilla coelebsCarpodacus synoicus
Chloris monguillotiCarpodacus thura
Crithagra mozambicaPyrrhula pyrrhulaSpinus cucullatusCarpodacus pulcherrimusProcarduelis nipalensis
Spinus tristisPyrrhula erythaca
Acanthis flammeaEophona migratoriaLinaria cannabinaLeucosticte tephrocotisCoccothraustes coccothraustes
Callacanthis burtoniRhodopechys sanguineus
Pyrrhula pyrrhulaEremopsaltria mongolica
Loxia leucopteraHaemorhous purpureus
Mycerobas carnipesBucanetes githagineusHesperiphona vespertina
Carpodacus roseusHeamorhous mexicanusCarpodacus synoicus
Euphonia xanthogasterLoxia pytyopsittacusErythrina erythrinaLoxia curvirostraCarpodacus rodochroaCarpodacus pulcherrimus
Procarduelis nipalensisCrithagra citrinelloidesHesperiphona vespertina
Carpodacus puniceusSpinus atratusMycerobas carnipes
Callacanthis burtoniPyrrhula erythacaCrithagra mennelli
Pinicola enucleatorParoreomyza montanaChlorophonia cyaneaCrithagra sulphurataEuphonia violaceaEuphonia chloroticaCarpodacus rhodochlamysHaematospiza sipahi
Carpodacus rodochroaEuphonia musicaLoxioides bailleuiEuphonia minuta
Carpodacus rubicilloidesEophona migratoriaCarpodacus sibiricus
Carpodacus pulcherrimusCarpodacus thuraAgraphospiza rubescensPinicola enucleatorCarpodacus puniceusHaematospiza sipahi
Carpodacus rubicilloidesCarposacus sibiricus
Carpodacus rubicillaCarpodacus rhodochlamys
-6 -4 -2 0 2 4 6 8
First component of PCA (sexual monomorphism → sexual dimorphism)
Carpodacus sibiricusEuphonia cayennensis
Euphonia laniirostrisCrithagra leucopygia
Agraphospiza rubescensEuphonia xanthogaster
Crithagra burtoniCrithagra striolata
Crithagra rufobrunneaChlorodrepanis virens
Spinus olivaceus
-6 -4 -2 0 2 4 6 8First component of PCA (migrants → residents)
Appendix S4. Supermatrix tree of Fringillidae for three nuclear introns and five mitochondrial genes.
S 4.1. Assembling the supermatrix
We downloaded all Fringillidae sequences in Genbank and sorted them by taxon and locus. After counting how many taxa were available per locus, we
decided to include in the supermatrix three introns and five mitochondrial genes (see locus list below), all of which were represented by at least 50
species. For each sequence, length, associated specimen/sample number and locality were retrieved from Genbank and/or the corresponding
publication and combined in a preliminary table. Possible misidentification or anomalous sequences were checked using simple neighbor-joining tree.
For each species we selected one sequence per locus. Whenever possible, for a given species we selected the sequences originated from the
same specimen or minimized the number of specimens, and we tried also to choose sequences obtained from the same subspecies or with similar
geographic origin.
Table S 4.1. Genes, alignment length and number of sequence per gene included in the supermatrix.
Locus Alignment length (bp) Number of sequences
Glyceraldehyde-3-phosphate dehydrogenase (GAPDH), intron 11 327 116 (68.6 %)
Myoglobin gene, intron 2 741 116 (68.69 %)
Ornithine decarboxylase (ODC) gene, introns 6-7 697 112 (66. %)
Cytochrome b (cytb) 1143 129 (76.3 %)
NADH dehydrogenase subunit II (ND2) 1041 133 (78.7 %)
NADH dehydrogenase subunit III (ND3) 351 129 (76.3 %)
Cytochrome oxidase subunit I (COI) 648 59 (34.9 %)
ATPase subunit 6 (ATP6) 684 81 (47.9 %)
Table S 4.2. Species and Genbank accession numbers included in the supermatrix.
Taxon Specimen GAPDH Myoglobin ODC cytb ND2 ND3 COI ATP6
Fringilla coelebs NRM 956301 JN715183 JN715273 JN715365 JN715455 JN715548
Fringilla teydea NHMO KU705760 KU705760 KU705760 KU705760 KU705760
Fringilla montifringilla NRM 20046395 JN715184 GU816941 GU816920 GU816851 GU816816
Chlorophonia cyanea NRM 20066989 JN715171 JN715263 JN715353 JN715537
Chlorophonia cyanea USNM 625305 JQ174424
Chlorophonia occipitalis no information EF529844
Chlorophonia occipitalis no information EF529956
Euphonia plumbea USNM 632543 JQ174819
Euphonia affinis 529-05 EU442311
Euphonia affinis no information EU442360
Euphonia luteicapilla USNM 612448 JQ174817
Euphonia chlorotica NRM 956750 JN715175 AY228298 JN715357 JN715448 JN715541
Euphonia finschi FMNH 389276 AF290143
Euphonia finschi NRM 20066306 JN715180 JN715270 JN715362 JN715545
Euphonia violacea NRM 966943 JN715181 JN715271 JN715363
JN715453 JN715546
Euphonia laniirostris LSU B18375 AF006232
Euphonia laniirostris LSU B18411
AF447330
Euphonia laniirostris NRM 20066309 JN715176 JN715266 JN715358 JN715449
Euphonia hirundinacea 528-15
EU442301
Euphonia hirundinacea no information
EU442333
Euphonia elegantissima KU 87070 JQ174807
Euphonia cyanocephala MACN-Or-ct 913
FJ027571
Euphonia musica no information AF310067
Euphonia musica NRM 976696 JN715178 JN715268 JN715360 JN715451 JN715543
Euphonia fulvicrissa STRI PAEFU102 AF383014 AF383130 AF382975
Euphonia gouldi CU 44255 FJ231698
Euphonia chrysopasta KU 89079 JQ174806
Euphonia minuta NRM 20066307 JN715177 JN715267 JN715359 JN715450 JN715542
Euphonia anneae USNM 607624 JQ174801
Euphonia xanthogaster NRM 20066305 JN715182 JN715272 JN715364 JN715454 JN715547
Euphonia rufiventris NRM 20066310 JN715179 JN715269 JN715361 JN715452 JN715544
Euphonia pectoralis MACN-Or-ct 2867 FJ027574
Euphonia cayennensis NRM 20056062 JN715174 JN715265 JN715356 JN715540
Mycerobas icterioides FMNH 256357 KJ456356
Mycerobas affinis AMNH 5592 KJ456354
Mycerobas melanozanthos FMNH 222122 KJ456357
Mycerobas carnipes NRM 23363 JN715196 JN715284 JN715376 JN715466 JN715558
Hesperiphona vespertina NRM 23336 JN715186 JN715275 JN715367
JN715457 JN715550
Hesperiphona vespertina UMMZ 235311
KM078770
KM078770 KM078770
Coccothraustes coccothraustes NRM 976374 JN715172 AY228292 JN715354 AY228055 JN715446 JN715538 GU571828
Eophona migratoria no information
AF342871
Eophona migratoria NRM 896473 JN715173 JN715264 JN715355
JN715447 JN715539
Eophona personata no information AF342872
Melamprosops phaeosoma BPBM 147112 KM112521 KM112827 KM078793 KM078793 KM078793 KM078793 KM078793
Paroreomyza montana NZP USFWS band 2141-67177
KM078771
KM078771 KM078771
Paroreomyza montana RCF 1984 JN715197 JN715285 JN715377
JN715467 JN715559
Dysmorodrepanis munroi NZP USFWS band 1581-75367 KM112533 KM112815 KM078774 KM078774 KM078774 KM078774 KM078774
Telespiza cantans NZP USFWS band 8061-85532 KM112508 KM112859 KM078777 KM078777 KM078777 KM078777 KM078777
Telespiza ultima Conant 92.7.26-1 KM112509 KM112811 KM078787 KM078787 KM078787 KM078787
Loxioides bailleui MRSNT 5783 JN715195 JN715283 JN715375
JN715465 JN715557
Loxioides bailleui NZP USFWS band 8031-75805
KM078805 KM078805
Psittirostra psittacea no information KU158196 KU158196 KU158196 KU158196 KU158196
Oreomystis bairdi MVZ 178406 KM112527 KC007674 KM112853 KM078807 KM078807 KM078807 KM078807 KM078807
Magumma parva MVZ 178407 KM112536 KM112805 KM078799 KM078799 KM078799 KM078799 KM078799
Loxops caeruleirostris MVZ 178405 KM112505 KM112834 KM078776 KM078776 KM078776 KM078776 KM078776
Loxops coccineus NZP USFWS band 2350-43262 KM112523 KM112807 KM078785 KM078785 KM078785 KM078785 KM078785
Manucerthia mana TKP 559 KM112532 KM112820 KM078768 KM078768 KM078768 KM078768 KM078768
Chlorodrepanis virens NZP RCF-3425
KM078788
KM078788 KM078788
Chlorodrepanis virens RCF 2913 JN715225 JN715313 JN715405
JN715496 JN715588
Chlorodrepanis flava NZP USFWS band 1680-10360 KM112537 KM112821 KM078780 KM078780 KM078780 KM078780 KM078780
Chlorodrepanis stejnegeri NZP RCF-2666 KM112512 KM112809 KM078801 KM078801 KM078801 KM078801 KM078801
Hemignathus wilsoni NZP RCF-3422 KM112535 KM112823 KM078802 KM078802 KM078802 KM078802 KM078802
Akialoa obscura no information KU158190 KU158190 KU158190 KU158190 KU158190
Pseudonestor xanthophrys NZP USFWS band 8051-40968 KM112541 KM112840 KM078809 KM078809 KM078809 KM078809 KM078809
Vestiaria coccinea NZP USFWS band 1471-19056 KM112546 KM112847 KM078797 KM078797 KM078797 KM078797 KM078797
Himatione sanguinea NZP RCF-3427 KM112501 KM112808 KM078773 KM078773 KM078773 KM078773 KM078773
Palmeria dolei BPBM 184556 KM112499 KM112801 KM078803 KM078803
Erythrina erythrina NRM 976373 JN715154 JN715246 JN715336
JN715428 JN715519 GU571800
Erythrina erythrina USNM B18937
KM078766
KM078766 KM078766
Haematospiza sipahi no information AF342875
Haematospiza sipahi NRM 23812 JN715185 JN715274 JN715366 JN715456 JN715549
Chaunoproctus ferreorostris BMNH 1855.12.19.71
JN715445 JN715536
Carpodacus synoicus MAR 5084 KF194098
Carpodacus synoicus NHMO 26633 JN715168 JN715260 JN715350 JN715442 JN715533
Carpodacus stoliczkae BMNH 1967.17803
KF194009
KF194103 KF194147
Carpodacus roborowskii NRM 23882 JN715161 JN715253 JN715343 JN715435 JN715526
Carpodacus rubicilloides MAR 5931
KF194089
Carpodacus rubicilloides NRM 23864 JN715167 JN715259 JN715349
JN715441 JN715532
Carpodacus rubicilla NRM 20016594 JN715166 JN715258 JN715348 JN715440 JN715531
Carpodacus rubicilla ZFMK J.II.22.f.l KF194088
Carpodacus sibiricus NRM 20076294 JN715224 JN715312 JN715404 JN715495 JN715587
Carpodacus sibiricus UWBM 47588 KM078763 KM078763 KM078763
Carpodacus puniceus FMNH 277071 KF194173
Carpodacus puniceus NRM 23927 JN715158 JN715250 JN715340 JN715432 JN715523
Carpodacus subhimachalus FMNH 277061 KF194180
Carpodacus subhimachalus NRM 23477 JN715199 JN715287 JN715379 JN715469 JN715561
Carpodacus roseus NRM 20026495 JN715164 JN715256 JN715346 JN715438 JN715529
Carpodacus roseus USNM B10230 KM078779 KM078779 KM078779
Carpodacus trifasciatus MTD C63834 KF194004 KF194019
KF194115 KF194166
Carpodacus thura AMNH DOT5609 KF194034 KJ455736 KF194181 KF194135
Carpodacus dubius MAR 369
KF194106
Carpodacus dubius NRM 20016581 JN715169 JN715261 JN715351
JN715443 JN715534
Carpodacus rhodochlamys NRM 20026491 JN715160 JN715252 JN715342 KF194174 JN715434 JN715525
Carpodacus grandis ZFMK J.II.22.g1.g KF194010 KF194051 KF194152
Carpodacus davidianus MTD C64235 KF193991 KF194018 KF194060 KF194156
Carpodacus pulcherrimus NRM 20026494 JN715157 JN715249 JN715339 KF194172 JN715431 JN715522
Carpodacus waltoni MAR 5936 KF193993 KF194017 KF194057 KF194141
Carpodacus edwardsii MTD C24119 KF194039
Carpodacus verreauxii CAS 95886
KF194033
KF194169 KF194128
Carpodacus verreauxii MNHN 19-37
EU880942
Carpodacus rodochroa AMNH DOT5671 KF194176
Carpodacus rodochroa NRM 553889 JN715162 JN715254 JN715344 JN715436 JN715527
Carpodacus rodopeplus RMNH 44517 JN715163 JN715255 JN715345
JN715437 JN715528
Carpodacus formosanus NMNST 7838 KF193996 KF194006 KF194119 KF194167
Carpodacus vinaceus MNHN 19.23
EU880943
Carpodacus vinaceus NRM 20026493 JN715170 JN715262 JN715352
JN715444 JN715535
Carpodacus vinaceus U Mainz MAR 961
HQ284695
Pinicola enucleator NRM 996174 JN715198 JN715286 JN715378 HQ284684 JN715468 JN715560 GU572046
Pyrrhula nipalensis MAR ES11
KF194184
Pyrrhula nipalensis NRM 23476 JN715202 JN715290 JN715382
JN715472 JN715564
Pyrrhula leucogenis CMC 36632 HQ284782 HQ284678
Pyrrhula aurantiaca BMNH 1949.25.3775
HQ284579
Pyrrhula erythrocephala MNHN 18-05 EU878710 EU881015 EU880949
Pyrrhula erythrocephala U Mainz MAR 90021 HQ284642
Pyrrhula erythaca NRM 20016568 JN715201 JN715289 JN715381 HQ284652 JN715471 JN715563
Pyrrhula murina U Sheffield TRB2 HQ284768 KX109679 KX109755 HQ284631 KX109700
Pyrrhula pyrrhula MNHN 95-25
EU880950
Pyrrhula pyrrhula NRM 20046541 JN715203 JN715291 JN715383
JN715473 JN715565 GU572069
Pyrrhula pyrrhula U Mainz MAR 4437
HQ284595
Rhodopechys sanguineus NRM 20026504 JN715207 JN715295 JN715387 JN715477 JN715569
Bucanetes githagineus MTD C64524 MAR1172
HQ284701
Bucanetes githagineus NRM 20046702 JN715204 JN715292 JN715384
JN715474 JN715566
Eremopsaltria mongolica NRM 23495 JN715205 JN715293 JN715385 JN715475 JN715567
Eremopsaltria mongolica USNM B10185 KM078792 KM078792 KM078792
Agraphospiza rubescens MART 90161
KF194120
Agraphospiza rubescens NRM 23826 JN715165 JN715257 JN715347
JN715439 JN715530
Callacanthis burtoni NRM 24869 JN715135 JN715227 JN715317 JN715409 JN715500
Pyrrhoplectes epauletta MNHN 16-2j
EU880948
Pyrrhoplectes epauletta MTD C63109 MAR5549
HQ284689
Pyrrhoplectes epauletta NRM 23810 JN715200 JN715288 JN715380
JN715470 JN715562
Procarduelis nipalensis no information AF342866
Procarduelis nipalensis NRM 23824 JN715156 JN715248 JN715338 JN715430 JN715521
Leucosticte nemoricola IZAS uncat JN715189 JN715278 JN715370 JN715460 JN715553
Leucosticte nemoricola MTD C62013 MAR4246 HQ284700
Leucosticte brandti NRM 24575 JN715188 JN715277 JN715369 JN715459 JN715552
Leucosticte brandti UWBM 66356 KM078775 KM078775 KM078775
Leucosticte sillemi ZMA.AVES 43449
KT444635
Leucosticte arctoa NRM 24559 JN715187 JN715276 JN715368 JN715458 JN715551
Leucosticte arctoa USNM 609762 KM078791 KM078791 KM078791
Leucosticte tephrocotis NRM 20016579 JN715190 JN715279 JN715371 JN715461
Leucosticte tephrocotis UWBM 66944 SVD 2371 KX109627
Haemorhous mexicanus NRM 20056140 JN715155 JN715247 JN715337
JN715429 JN715520
Haemorhous mexicanus NZP RCF-2645
KM078782
KM078782 KM078782
Haemorhous cassinii USNM B20075 KM112518 KM112813 KM078786 KM078786 KM078786 KM078786 KM078786
Haemorhous purpureus NRM 557743 JN715159 JN715251 JN715341
JN715433 JN715524
Haemorhous purpureus UMMZ 227048 T-126
KM078772
KM078772
Rhodospiza obsoleta NRM 20046707 JN715206 JN715294 JN715386 JN715476 JN715568
Rhynchostruthus socotranus NRM 23483 JN715208 JN715296 JN715388
JN715478 JN715570
Chloris chloris MNHN C34 EU880931
Chloris chloris NRM 986328 JN715141 JN715233 JN715323
JN715415 JN715506 GU571791
Chloris chloris SMTD C 62175 HQ284692
Chloris sinica NRM 20026538 JN715150 JN715242 JN715332
JN715424 JN715515
Chloris sinica USNM B19440
KM078783
KM078783 KM078783
Chloris spinoides NRM 20026503 JN715151 JN715243 JN715333 KJ456211 JN715425 JN715516
Chloris spinoides ZMUC 131646 EU880974
Chloris monguilloti NRM 546196 JN715147 JN715239 JN715329
JN715421 JN715512
Chloris ambigua no information U78322
Chloris ambigua NRM 20026539 JN715136 JN715228 JN715318
JN715410 JN715501
Chloris ambigua ZMUC 118651 EU880992
Linurgus olivaceus MNHN 40-23
EU880938
Linurgus olivaceus NRM 20086232 JN715191 JN715280 JN715372
JN715462 JN715554
Crithagra citrinelloides no information AY790888
Crithagra citrinelloides NRM 20026501 JN715212 JN715300 JN715392
JN715482 JN715574
Crithagra citrinelloides ZMUC 134740 EU880968
Crithagra hyposticta ZMUC 131127
EU878731
EU881039
EU880971
Crithagra capistrata ZMUC 135500 EU878742 EU881052 EU880984
Crithagra scotops no information
AY790894
Crithagra leucopygia no information L76264
Crithagra leucopygia NRM 20106050 JN715214 JN715302 JN715394
JN715485 JN715577
Crithagra leucopygia ZMUC 118662 EU880993
Crithagra atrogularis no information
L76267
Crithagra citrinipectus ZMUC 130559 EU878717 EU881025 EU880957
Crithagra mozambica MNHN 40-54
EU880953
Crithagra mozambica no information
L76265
Crithagra mozambica NRM 20066026 JN715216 JN715304 JN715396
JN715487 JN715579
Crithagra flaviventris no information AY790887
Crithagra flaviventris ZMUC 132129 EU878732 EU881040 EU880972
Crithagra dorsostriata UMMZ 233806 T-810c KM112547
KM112837 KM078798 KM078798 KM078798 KM078798 KM078798
Crithagra sulphurata no information AY790889
Crithagra sulphurata NRM 20026498 JN715221 JN715309 JN715401 JN715492 JN715584
Crithagra albogularis UWBM 70375 KM112520
KM112836 KM078764 KM078764 KM078764 KM078764 KM078764
Crithagra reichardi ZMUC 122436 EU878734 EU881043 EU880975
Crithagra gularis no information
L77556
Crithagra gularis ZMUC 131650
EU881041
EU880973
Crithagra mennelli NRM 20026500 JN715215 JN715303 JN715395 JN715486 JN715578
Crithagra mennelli ZMUC 118671 EU880990
Crithagra striolata no information
AY790895
Crithagra striolata NRM 23718 JN715220 JN715308 JN715400
JN715491 JN715583
Crithagra striolata ZMUC 134756
EU880969
Crithagra burtoni no information AY790896
Crithagra burtoni NRM 20086267 JN715209 JN715297 JN715389
JN715479 JN715571
Crithagra burtoni ZMUC 123647 EU880997
Crithagra melanochroa ZMUC 118856
EU878737
EU881046
EU880978
Crithagra rufobrunnea NRM 857618 JN715218 JN715306 JN715398 JN715489 JN715581
Crithagra totta no information
AY790892
Linaria flavirostris JM136 KJ456172
Linaria flavirostris NRM 20066634 JN715144 JN715236 JN715326 JN715418 JN715509 GU571794
Linaria cannabina MNHN 25-82
EU880939
Linaria cannabina NRM 966403 JN715139 JN715231 JN715321
JN715413 JN715504 GU571787
Linaria cannabina SMTD C 61033
HQ284691
Acanthis flammea no information L76386
Acanthis flammea NRM 20016449 JN715143 JN715235 JN715325 JN715417 JN715508 GU571793
Acanthis hornemanni AJN 000043 JN715145 JN715237 JN715327
JN715419 JN715510 GU571795
Acanthis hornemanni no information
U83201
Acanthis hornemanni ZMUC 119818
EU880989
Loxia pytyopsittacus NRM 20046001 JN715194 JN715282 JN715374 JN715464 JN715556 GU571962
Loxia pytyopsittacus ZMUC 119824 EU880986
Loxia scotica no information
AF171656
Loxia curvirostra NRM 976546 JN715192 AY228303 GU816921 AY228065 GU816852 GU816817 GU571958
Loxia leucoptera no information
AF342878
Loxia leucoptera NRM 20026565 JN715193 JN715281 JN715373
JN715463 JN715555 GU571960
Loxia leucoptera ZMUC 116705
EU880962
Chrysocorythus estherae RMNH 44712 JN715483 JN715575
Carduelis carduelis NRM 996076 JN715140 JN715232 JN715322
JN715414 JN715505 GU571789
Carduelis carduelis NZP USFWS band 1760-76299
KM078790 KM078790
Carduelis citrinella MNHN C38 EU880933
Carduelis citrinella no information
L77872
Carduelis citrinella NRM 553307 JN715211 JN715299 JN715391 JN715481 JN715573
Serinus serinus no information
L76263
Serinus serinus NRM 20046491 JN715219 JN715307 JN715399
JN715490 JN715582 GU572089
Serinus serinus ZMUC 116715
EU880980
Serinus canaria NRM 20026502 JN715213 JN715301 JN715393 JN715484 JN715576
Serinus canaria NZP 105 KM078794 KM078794 KM078794
Serinus syriacus NRM 23600 JN715222 JN715310 JN715402
JN715493 JN715585
Serinus pusillus JM128 KJ456465
Serinus pusillus NRM 20046715 JN715217 JN715305 JN715397
JN715488 JN715580
Serinus pusillus ZMUC 135626 EU880983
Serinus alario no information
AY790899
Serinus canicollis no information AY790890
Serinus canicollis NRM 20076189 JN715210 JN715298 JN715390
JN715480 JN715572
Serinus canicollis ZMUC 128624 EU880958
Serinus flavivertex no information
AY790897
Spinus thibetanus BMNH 1948.34.64 JN715223 JN715311 JN715403 JN715494 JN715586
Spinus thibetanus no information L76279
Spinus spinus MNHN 2000.1651
EU880941
Spinus spinus no information
L76391
Spinus spinus NRM 986184 JN715152 JN715244 JN715334
JN715426 JN715517 GU571799
Spinus pinus NRM 20016375 JN715148 JN715240 JN715330 JN715422 JN715513
Spinus pinus UMMZ 227858 KM078796 KM078796 KM078796
Spinus tristis MSB 29161
KT221304
Spinus tristis NRM 20016378 JN715153 JN715245 JN715335
JN715427 JN715518
Spinus psaltria NRM 20016376 JN715149 JN715241 JN715331 JN715423 JN715514
Spinus psaltria NZP USFWS band 2120-99480 KM078806 KM078806 KM078806
Spinus lawrencei MVZ 176985
KT221368
KT221302 KT221172
Spinus atriceps 01N6050 KT358782
Spinus atriceps AMNH DOT7151 KT221375 KT221309 KT221179 KT221243
Spinus spinescens ANSP 18807
KT221360 KT221230 KT221294
Spinus spinescens ZMUC 120509
EU880985
Spinus yarrellii no information U83200
Spinus cucullatus NRM 20026508 JN715142 JN715234 JN715324
JN715416 JN715507
Spinus cucullatus USNM B12867
KT221318
Spinus cucullatus ZMUC 135619
EU880982
Spinus crassirostris MSB 34207 KT221383 KT221317 KT221187 KT221251
Spinus crassirostris ZMUC 129671 EU880959
Spinus magellanicus FMNH 334723
KT221349
Spinus magellanicus NRM 986696 JN715146 JN715238 JN715328
JN715420 JN715511
Spinus magellanicus ZMUC 120822
EU880988
Spinus dominicensis AMNH DOT6930 KT221387 KT221322 KT221192 KT221256
Spinus siemiradzkii ANSP 19701
KT221358
Spinus siemiradzkii ZMUC 116681
EU878725
EU881033
EU880965
Spinus olivaceus ANSP 19746 KT221354 KT221224 KT221288
Spinus notatus 03N1083
KT358784
Spinus notatus FMNH 393899
KT221417
KT221352 KT221222 KT221286
Spinus xanthogastrus ANSP 18543 KT221365
Spinus xanthogastrus ZMUC 116687 EU878721 EU881029 EU880961
Spinus atratus MSB 34123
KT221305
Spinus atratus NRM 546071 JN715137 JN715229 JN715319
JN715411 JN715502
Spinus atratus ZMUC 118878
EU880994
Spinus uropygialis MSB 33471 KT221422 KT221364 KT221234 KT221298
Spinus uropygialis ZMUC 116685 EU880964
Spinus barbatus AMNH DOT10430 KT221310
Spinus barbatus NRM 546142 JN715138 JN715230 JN715320 JN715412 JN715503
100
10090
Fringilla coelebsFringilla teydea
Fringilla montifringilla
100
99
99
94
96Haemorhous mexicanus
100Haemorhous cassinii
Haemorhous purpureus
98
100100
Chloris chloris
91Chloris sinica
100Chloris ambigua
53Chloris spinoides
Chloris monguilloti
100Rhodospiza obsoleta
Rhynchostruthus socotranus
89
95
Linurgus olivaceus
83
29
Crithagra rufobrunnea
23
82Crithagra dorsostriata
83Crithagra mozambica
99Crithagra citrinipectus
96Crithagra atrogularis
Crithagra leucopygia
24Crithagra scotops
100Crithagra capistrata
95Crithagra hypostictaCrithagra citrinelloides
16
17Crithagra burtoni
26Crithagra totta
69Crithagra striolata
Crithagra melanochroa
9897
Crithagra albogularis
100Crithagra flaviventris
Crithagra sulphurata
99Crithagra reichardi
89Crithagra gularis
Crithagra mennelli
52
100100
Loxia leucoptera
100Loxia pytyopsittacus
94Loxia scotica
Loxia curvirostra
100Acanthis hornemanniAcanthis flammea
90
99Linaria flavirostrisLinaria cannabina
31
59
97
Spinus thibetanus
81
100
100
Spinus notatus
100
Spinus cucullatus
49
Spinus barbatus
31
60Spinus olivaceus
Spinus spinescens
1257
Spinus uropygialis
98Spinus siemiradzkii
Spinus crassirostris
19Spinus xanthogastrus
16Spinus atratus
48Spinus yarrellii
Spinus magellanicus
82Spinus dominicensis
91Spinus spinus
100Spinus atriceps
Spinus pinus
99Spinus tristis
69Spinus psaltria
Spinus lawrencei
9999
Serinus alario
2483
Serinus syriacusSerinus pusillus
97Serinus canicollis
Serinus flavivertex
100Serinus serinus
Serinus canaria
67Chrysocorythus estherae
91Carduelis carduelis
Carduelis citrinella
32
81
98
Pinicola enucleator
98
Pyrrhula nipalensis
98
Pyrrhula leucogenis
58100
Pyrrhula pyrrhulaPyrrhula murina
48Pyrrhula aurantiaca
88Pyrrhula erythaca
Pyrrhula erythrocephala
60
98
89Agraphospiza rubescens
100Pyrrhoplectes epauletta
Callacanthis burtoni
100Procarduelis nipalensis
90Leucosticte nemoricola
100Leucosticte brandti
100Leucosticte arctoa
Leucosticte tephrocotis
100Rhodopechys sanguineus
100Eremopsaltria mongolica
Bucanetes githagineus
75
81
100Haematospiza sipahiErythrina erythrina
77
Chaunoproctus ferreorostris
69
18
70
100Carpodacus grandis
Carpodacus rhodochlamys
46
98Carpodacus waltoni
96Carpodacus pulcherrimus
Carpodacus davidianus
44
Carpodacus edwardsii
8199
Carpodacus rodochroaCarpodacus verreauxii
70Carpodacus rodopeplus
94Carpodacus formosanus
Carpodacus vinaceus
100Carpodacus rubicilloides
Carpodacus rubicilla
34
32100 Carpodacus stoliczkae
Carpodacus synoicus
100Leucosticte sillemi
Carpodacus roborowskii
6397 Carpodacus subhimachalus
Carpodacus puniceus
32Carpodacus sibiricus
100Carpodacus roseus
100Carpodacus trifasciatus
100Carpodacus thura
Carpodacus dubius
99
Melamprosops phaeosoma
100
100
46
Akialoa obscura
35
69
94100
Manucerthia mana
94Loxops caeruleirostris
Loxops coccineus
100Chlorodrepanis stejnegeri
50Chlorodrepanis flava
100Chlorodrepanis virensHemignathus wilsoni
37Pseudonestor xanthophrys
21Dysmorodrepanis munroi
Magumma parva
28Psittirostra psittacea
100Vestiaria coccinea
55Palmeria dolei
Himatione sanguinea
75Loxioides bailleui
100Telespiza ultima
Telespiza cantans
64 Oreomystis bairdiParoreomyza montana
100
55Coccothraustes coccothraustes
Hesperiphona vespertina
3197
Mycerobas melanozanthos
99Mycerobas icterioides
Mycerobas affinis
45Mycerobas carnipes
100Eophona personata
Eophona migratoria
99
36
25
31
49Euphonia chrysopasta
75Euphonia anneae
Euphonia pectoralis
9295 Euphonia finschi
Euphonia chlorotica
36Euphonia affinis
95Euphonia luteicapilla
Euphonia plumbea
85
97100
Euphonia gouldiEuphonia fulvicrissa
56Euphonia xanthogaster
99Euphonia cayennensis
Euphonia rufiventris
81Euphonia minuta
86Euphonia hirundinacea
99Euphonia laniirostris
Euphonia violacea
45Chlorophonia occipitalis
80Chlorophonia cyanea
Euphonia musica
100Euphonia elegantissima
Euphonia cyanocephala
100Plectrophenax nivalis
91Ammodramus humeralis
68Parula pitiayumi
Leistes superciliaris
100100
Motacilla albaAnthus trivialis
10096
Petronia petroniaMontifringilla ruficollis
100Passer luteus
Passer montanus
©M
rEnt