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:ponge@mnhn.fr

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

9936  |     PONGE Et al.

(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

     |  9937PONGE Et al.

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

9938  |     PONGE Et al.

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

0.2

0.4

0.6

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

–0.8

–0.6

–0.4

–0.2

0.0

0.2

0.4

0.6

0.8

1.0

–1.0 –0.8 –0.6 –0.4 –0.2 0.0 0.2 0.4 0.6 0.8 1.0PC1 (36%)

PC2

(23%

)

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

–0.8

–0.6

–0.4

–0.2

0.0

0.2

0.4

0.6

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

PC1 (28%)

PC2

(13%

)

Nests dispersed

Breeding dispersion

Breeding dispersion plasticity

Territorial

Gregariousness

Gregariousness plasticity

Mixed partiesMigration

Migration plasticity

–1.0

–0.8

–0.6

–0.4

–0.2

0.0

0.2

0.4

0.6

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

PC1 (36%)

PC2

(15%

)

(a) (b)

(c) (d)

     |  9939PONGE Et al.

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

9940  |     PONGE Et al.

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

REFERENCES

Abouheif,E.(1999).Amethodfortestingtheassumptionofphylogeneticindependenceincomparativedata.Evolutionary Ecology Research,1(8),895–909.

Badyaev, A. V. (1997a). Covariation between life history and sexuallyselected traits: An example with cardueline finches. Oikos, 80(1),128–138.

Badyaev,A.V.(1997b).Avianlifehistoryvariationalongaltitudinalgradi-ents:Anexamplewithcarduelinefinches.Oecologia,111(3),365–374.

Badyaev,A.V. (1997c).Altitudinalvariation insexualdimorphism:Anewpatternandalternativehypotheses.Behavioral Ecology,8(6),675–690.

Badyaev,A.V.,&Ghalambor,C.K.(1998).Doesatrade-offexistbetweensexual ornamentation and ecological plasticity? Sexual dichromatismandoccupiedelevationalrangeinfinches.Oikos,82(2),319–324.

Badyaev,A.V.,Hill,G.E.,&Weckworth,B.V.(2002).Speciesdivergenceinsexuallyselectedtraits:Increaseinsongelaborationisrelatedtode-creaseinplumageornamentationinfinches.Evolution,56(2),412–419.

Bailey,S.F.(1978).Latitudinalgradientsincolorsandpatternsofpasserinebirds.Condor,80(4),372–381.

Barnagaud,J.Y.,Devictor,V.,Jiguet,F.,&Archaux,F.(2011).Whenspeciesbecomegeneralists:On-goinglarge-scalechangesinbirdhabitatspe-cialization.Global Ecology and Biogeography,20(4),630–640.

Beckman,E.J.,&Witt,C.C. (2015).PhylogenyandbiogeographyoftheNewWorldsiskinsandgoldfinches:Rapid,recentdiversificationintheCentralAndes.Molecular Phylogenetics and Evolution,87,28–45.

Berg,M.P.,Kiers,T.,Driessen,G.,VanderHeijden,M.,Kooi,B.W.,Kuenen,F.,…Ellers,J. (2010).Adaptordisperse:Understanding speciesper-sistenceinachangingworld.Global Change Biology,16(2),587–598.

Blanck,A.,Tedesco,P.A.,&Lamouroux,N.(2007).Relationshipsbetweenlife-history strategies of European freshwater fish species and theirhabitatpreferences.Freshwater Biology,52(5),843–859.

Bonte, D.,VanDyck, H., Bullock, J.M., Coulon,A., Delgado,M., Gibbs,M.,…Travis,J.M.(2012).Costsofdispersal.Biological Reviews,87(2),290–312.

Borics,G.,Várbiró,G.,&Padisák,J.(2013).Disturbanceandstress:Differentmeaningsinecologicaldynamics?Hydrobiologia,711(1),1–7.

Botero,C.A.,&Rubenstein,D.R.(2012).Fluctuatingenvironments,sexualselectionandtheevolutionofflexiblematechoiceinbirds.PLoS ONE,7(2),e32311.

Brown,W.L.Jr,&Wilson,E.O.(1956).Characterdisplacement.Systematic Zoology,5(2),49–64.

Brumfield,R.T.,Tello,J.G.,Cheviron,Z.A.,Carling,M.D.,Crochet,N.,&Rosenberg, K.V. (2007). Phylogenetic conservatism and antiquity ofa tropical specialization: Army ant-following in the typical antbirds(Thamnophilidae).Molecular Phylogenetics and Evolution,45(1),1–13.

Cardillo,M.(2002).Thelife-historybasisoflatitudinaldiversitygradients:Howdospecies traitsvary from thepoles to theequator. Journal of Animal Ecology,71(1),79–87.

Clement, P.,Harris,A.,&Davis, J. (2011).Finches and sparrows (p. 512).London:Bloomsbury.

Dickinson, E. C., & Christidis, L. (2014). The Howard and Moore com-plete checklist of the birds of the World. II. Passerines (752pp,4thed.).Eastbourne:AvesPress.

Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionaryanalysisbysamplingtrees.BMC Evolutionary Biology,7(1),214.

Flegr,J.(1997).Twodistincttypesonnaturalselectioninturbidostat-likeandchemostat-likeecosystems.Journal of Theoretical Biology,188(1),121–126.

Friedman, N. R., Hofmann, C. M., Kondo, B., & Omland, K. E. (2009).CorrelatedevolutionofmigrationandsexualdichromatismintheNewWordorioles(Icterus).Evolution,63(12),3269–3274.

Greenslade,P.J.M. (1983).Adversity selectionand thehabitat templet.American Naturalist,122(3),352–365.

Griffith, S. C., Parker, T. H., & Olson, V. A. (2006). Melanin- versuscarotenoid-basedsexual signals: Is thedifference reallysoblackandred?Animal Behaviour,71,749–763.

Harmon,L.J.,Weir,J.T.,Brock,C.D.,Glor,R.E.,&Challenger,W.(2008).GEIGER: Investigating evolutionary radiations. Bioinformatics, 24(1),129–131.

Hill,G.E.(1990).Femalehousefinchesprefercolourfulmales:Sexualselec-tionforacondition-dependenttrait.Animal Behaviour,40(3),563–572.

Holmes,C.C.,&Adams,N.M. (2002).Aprobabilisticnearestneighbourmethodforstatisticalpatternrecognition.Journal of the Royal Statistical Society, Series B, Statistical Methodology,64(2),295–306.

Hwang,W.S.,&Weirauch,C.(2012).Evolutionaryhistoryofassassinbugs(Insecta:Hemiptera:Reduviidae):Insightsfromdivergencedatingandancestralstatereconstruction.PLoS ONE,7(9),e45523.

Janzen, D. H. (1967). Why mountain passes are higher in the tropics.American Naturalist,101,233–249.

Jetz,W.,Freckleton,R.P.,&MvKechnie,A.E.(2008).Environment,migra-torytendency,phylogenyandbasalmetabolicrateinbirds.PLoS ONE,3(9),e3261.

Jombart,T.,Pavoine,S.,Devillard,S.,&Pontier,D.(2010).Puttingphylog-eny into theanalysisofbiological traits:Amethodological approach.Journal of Theoretical Biology,264(3),693–701.

Jones,J.M.(1976).Ther-K-selectioncontinuum.American Naturalist,110,320–323.

Jønsson,K.A.,Fabre,P.H.,Ricklefs,R.E.,&Fjeldså,J.(2011).Majorglobalradiationofcorvoidbirdsoriginatedintheproto-Papuanarchipelago.Proceedings of the National Academy of Sciences of the United States of America,108(6),2328–2333.

Kelley,S.T.,&Farrell,B.D.(1998).Isspecializationadeadend?Thephy-logenyofhostuseinDendroctonusbarkbeetles(Scolytidae).Evolution,52(6),1731–1743.

Laiolo,P.,Seoane,J.,Illera,J.C.,Bastianelli,G.,Carrascal,L.M.,&Obeso,J.R.(2015).Theevolutionaryconvergenceofavianlifestylesandtheirconstrainedcoevolutionwithspecies’ecologicalniche.Proceedings of the Royal Society of London, Series B, Biological Sciences,282,20151808.

Lerner,H.R.L.,Meyer,M.,James,H.F.,Hofreiter,M.,&Fleischer,R.C.(2011).MultilocusresolutionofphylogenyandtimescaleintheextantadaptiveradiationofHawaiianhoneycreepers.Current Biology,21(21),1838–1844.

Loiseau,C.,Harrigan,R.J.,Robert,A.,Bowie,R.C.K.,Thomassen,H.A.,Smith,T.B.,&Sehgal,R.N.M.(2012).HostandhabitatspecializationofavianmalariainAfrica.Molecular Ecology,21(2),431–441.

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010).Creating the CIPRESScienceGatewayforinferenceoflargephylogenetictrees.InGatewayComputing Environments Workshop (GCE 2010), Proceedings of ameeting held on 14 November 2010, NewOrleans, LA. Red Hook,Curran Associates. Retrieved from http://ai2-s2-pdfs.s3.amazonaws.com/e27a/caf97f5b2eae4257bb5d8278fbe0e6405c39.pdf,7pp.

Møller,A.P.,&Garamszegi,L.Z. (2012).Sexualselection,rangesizeandpopulationsize.Ornis Hungarica,20(1),1–25.

Pagel,M.,&Meade,A. (2006).Bayesiananalysisof correlatedevolutionofdiscretecharactersbyreversible-jumpMarkovchainMonteCarlo.American Naturalist,167(6),808–825.

Pagel,M.,Meade,A.,&Barker,D.(2004).Bayesianestimationofancestralcharacterstatesonphylogenies.Systematic Biology,53(5),673–684.

Pavoine,S.,Ollier,S.,Pontier,D.,&Chessel,D.(2008).Testingforphyloge-neticsignalinphenotypictraits:Newmatricesofphylogeneticproxim-ities.Theoretical Population Biology,73(1),79–91.

     |  9953PONGE Et al.

Peterson,A.T.,Soberón,J.,&Sánchez-Cordero,V. (1999).Conservatismofecologicalnichesinevolutionarytimes.Science,285,1265–1267.

Poisot,T.,Bever,J.D.,Nemri,A.,Thrall,P.H.,&Hochberg,M.E. (2011).Aconceptualframeworkfortheevolutionofecologicalspecialization.Ecology Letters,14(9),841–851.

Ponge, J. F. (2013). Disturbances, organisms and ecosystems: A globalchangeperspective.Ecology and Evolution,3(4),1113–1124.

Posada,D.,&Crandall,K.A.(2001).Selectingthebest-fitmodelofnucleo-tidesubstitution.Systematic Biology,50(4),580–601.

Price,J.J.,Lanyon,S.M.,&Omland,K.E. (2009).Lossesoffemalesongwithchangesfromtropicaltotemperatebreeding intheNewWorldblackbirds.Proceedings of the Royal Society of London, Series B, Biological Sciences,276,1971–1980.

Prinzing,A.,D’Haese,C.,Pavoine,S.,&Ponge,J.F.(2014).SpecieslivinginharshenvironmentshavelowcladerankandarelocalizedonformerLaurasiancontinents:AcasestudyofWillemia(Collembola).Journal of Biogeography,41(2),353–365.

Prinzing,A.,Durka,W.,Klotz,S.,&Brandl,R.(2001).Thenicheofhigherplants: Evidence for phylogenetic conservatism. Proceedings of the Royal Society of London, Series B, Biological Sciences,268,2383–2389.

RCoreTeam(2016).R: A language and environment for statistical computing. Vienna:RFoundationforStatisticalComputing.Retrievedfromhttp://www.R-project.org/

Raia, P., Carotenuto, F., Passaro, F., Fulgione,D., & Fortelius,M. (2012).Ecological specialization in fossil mammals explains Cope’s rule.American Naturalist,179(3),328–337.

Rottenberg, H. (2007). Exceptional longevity in songbirds is associatedwithhighratesofevolutionofcytochromeb,suggestingselectionforreduced generation of free radicals. Journal of Experimental Biology,210(12),2170–2180.

Roulin, A. (2015). Condition-dependence, pleiotropy and the handicapprinciple of sexual selection inmelanin-based colouration.Biological Reviews,91(2),328–348.

Safran, R. J.,McGraw,K. J.,Wilkins,M.R.,Hubbard, J. K.,&Marling, J.(2010).Positivecarotenoidbalancecorrelateswithgreaterreproduc-tiveperformanceinawildbird.PLoS ONE,5(2),e9420.

Sallan, L.,&Galimberti,A.K. (2015). Body-size reduction invertebratesfollowingtheend-Devonianmassextinction.Science,350,812–815.

Schmeller,D. S.,Henle,K., Loyau,A.,Besnard,A.,&Henry,P.Y. (2012).Bird-monitoring inEurope:A firstoverviewofpractices,motivationsandaims.Nature Conservation,2,41–57.

Schneeweiss,G.M. (2007).Correlatedevolutionof lifehistory andhostrange in thenonphotosyntheticparasitic floweringplantsOrobanche andPhelipanche(Orobanchaceae).Journal of Evolutionary Biology,20(2),471–478.

Sedivy,C.,Praz,C.J.,Müller,A.,Widmer,A.,&Dorn,S.(2008).Patternsofhost-plantchoiceinbeesofthegenusChelostoma:Theconstrainthypothesisofhost-rangeevolutioninbees.Evolution,62(10),2487–2507.

Sheldon, P. R. (1996). Plus ça change: A model for stasis and evolu-tion in different environments. Palaeogeography, Palaeoclimatology, Palaeoecology,127(1),209–227.

Shutler,D.,&Weatherhead,P.J.(1990).Targetsofsexualselection:Songandplumageofwoodwarblers.Evolution,44(8),1967–1977.

Sih,A.,Bell,A.,&Johnson,J.C.(2004).Behavioralsyndromes:Anecolog-icalandevolutionaryoverview.Trends in Ecology and Evolution,19(7),372–378.

Simpson,R.K.,Johnson,M.A.,&Murphy,T.G.(2015).Migrationandtheevolution of sexual dichromatism: Evolutionary loss of female color-ationwithmigration amongwood-warblers.Proceedings of the Royal Society of London, Series B, Biological Sciences,282,20150375.

Smith, B. T., Bryson, R. W. Jr, Chua, V., Africa, L., & Klicka, J. (2013).Speciational history of North American Haemorhous finches (Aves:Fringillidae)inferredfrommultilocusdata.Molecular Phylogenetics and Evolution,66(3),1055–1059.

Sol,D.,Garcia,N.,Iwaniuk,A.,Davis,K.,Meade,A.,Boyle,W.A.,&Székely,T.(2010).Evolutionarydivergenceinbrainsizebetweenmigratoryandresidentbirds.PLoS ONE,5(3),e9617.

Southwood,T.R.E.,May,R.M.,Hassell,M.P.,&Conway,G.R. (1974).Ecological strategies andpopulationparameters.American Naturalist,108,791–804.

Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-basedphylogenetic analyses with thousands of taxa and mixed models.Bioinformatics,22(21),2688–2690.

Steinhaus, H. (1956). Sur la division des corps matériels en parties.Bulletin de l’Académie Polonaise des Sciences, Classe Troisième,4(12),801–804.

Stevens,V.M.,Whitmee,S.,LeGalliard,J.F.,Clobert,J.,Böhning-Gaese,K.,Bonte,D.,…Baguette,M.(2014).Acomparativeanalysisofdispersalsyndromes in terrestrial and semi-terrestrial animals.Ecology Letters,17(8),1039–1052.

Stireman,J.O.III (2005).Theevolutionofgeneralization?Parasitoidfliesand the perils of inferring host range evolution from phylogenies.Journal of Evolutionary Biology,18(2),325–336.

Tarof, S., Dunn, P.O., &Whittingham, L.A. (2005). Dual functions of amelanin-based ornament in the common yellowthroat. Proceedings of the Royal Society of London, Series B, Biological Sciences, 272, 1121–1127.

Tietze, D. T., Päckert, M., Martens, J., Lehmann, H., & Sun, Y. H. (2013).Completephylogenyandhistoricalbiogeographyoftruerosefinches(Aves:Carpodacus).Zoological Journal of the Linnean Society,169(1),215–234.

Töpfer, T., Haring, E., Birkhead, T. R., Lopes, R. J., Severinghaus, L. L.,Martens,J.,&Päckert,M.(2011).AmolecularphylogenyofbullfinchesPyrrhulaBrisson,1760(Aves:Fringillidae).Molecular Phylogenetics and Evolution,58(2),271–282.

Tripp,E.A.,&Manos,P.S. (2008). Isfloralspecializationanevolutionarydead-end? Pollination system transitions in Ruellia (Acanthaceae).Evolution,62(7),1712–1737.

Wiens,J.J.,&Graham,C.H.(2005).Nicheconservatism:Integratingevo-lution,ecology,andconservationbiology.Annual Review of Ecology and Systematics,36,519–539.

Wiersma,P.,Muñoz-Garcia,A.,Walker,A.,&Williams,J.B.(2007).Tropicalbirdshaveaslowpaceof life.Proceedings of the National Academy of Sciences of the United States of America,104(22),9340–9345.

Wiersma,P.,Nowak,B.,&Williams,J.B.(2012).Smallorgansizecontrib-utes to theslowpaceof life in tropicalbirds.Journal of Experimental Biology,215(10),1662–1669.

Yotoko, K. S. C., & Elisei, C. (2006). Malaria parasites (Apicomplexa,Haematozoea)andtheirrelationshipswiththeirhosts:Isthereanevo-lutionary cost for the specialization? Journal of Zoological Systematics and Evolutionary Research,44(4),265–273.

Zuccon,D.,Prŷs-Jones,R.,Rasmussen,P.C.,&Ericson,P.G.P.(2012).Thephylogenetic relationships and generic limits of finches (Fringillidae).Molecular Phylogenetics and Evolution,62(2),581–596.

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