A new time tree reveals Earth history s imprint on the...

R E S EARCH ART I C L E

EVOLUT IONARY ECOLOGY

Department of Ornithology, American Museum of Natural History, Central Park Westat 79th Street, New York, NY 10024, USA.*Corresponding author. E-mail: [email protected] (S.C.); [email protected] (J.C.)

Claramunt and Cracraft Sci. Adv. 2015;1:e1501005 11 December 2015

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10.1126/sciadv.1501005

A new time tree reveals Earth history’s imprint onthe evolution of modern birds
Santiago Claramunt* and Joel Cracraft*
Determining the timing of diversification of modern birds has been difficult. We combined DNA sequences of clock-like genes for most avian families with 130 fossil birds to generate a new time tree for Neornithes and investigatedtheir biogeographic and diversification dynamics. We found that the most recent common ancestor of modern birdsinhabited South America around 95 million years ago, but it was not until the Cretaceous-Paleogene transition(66 million years ago) that Neornithes began to diversify rapidly around the world. Birds used two main dis-persion routes: reaching the Old World through North America, and reaching Australia and Zealandia throughAntarctica. Net diversification rates increased during periods of global cooling, suggesting that fragmentationof tropical biomes stimulated speciation. Thus, we found pervasive evidence that avian evolution has beeninfluenced by plate tectonics and environmental change, two basic features of Earth’s dynamics.

INTRODUCTION

Modern birds (Neornithes) are the most diverse group of terrestrialvertebrates in terms of their species richness and global distribution,yet we still have a poor understanding of their large-scale evolutionaryhistory. Major advances in our knowledge of phylogenetic relationshipshave been made over the last decade (1–4), but the lack of a robust timetree, along with a comprehensive quantitative biogeographic analysis,has hindered progress toward a better understanding of the process ofdiversification in modern birds.

Determining the timing of avian diversification has been difficult.There is now a broad agreement that modern birds originated some-time in the Cretaceous (3, 5–8), but actual molecular age estimates varyfrom 72 mega-annum (Ma) (4) to 170 Ma (5), and fossils of indisputableneornithine affinities have only been found in the latest Cretaceous,about 67 Ma ago (9). Similarly, there is no agreement on the timingof diversification within the three major avian groups: Palaeognathae(tinamous and ratites), Galloanseres (waterfowl, pheasants, and allies),and the megadiverse Neoaves (all other birds); whereas most molecularestimates date the early radiation within these groups before the Cretaceous-Paleogene (K-Pg) transition (5, 7, 10–14), with very few exceptionsfossils have been found only after the K-Pg extinction event (6, 15–17).The possibility of a rapid post–K-Pg radiation of birds has led some tosuggest a major effect of ecological opportunity on avian diversifica-tion due to the extinction of major competitors [the “big bang” model(13, 15)]. The big-bang model of avian diversification has received re-newed attention because some recent molecular time trees recoveredthe rapid radiation of Neoaves as coinciding with the K-Pg event (3–5, 7);among them, time trees inferred using genomic data represent an im-portant advancement because they overcame several drawbacks ofprevious analyses by using hundreds of loci and 19 fossil calibrationsin Bayesian relaxed-clock analyses (3, 4). Previous estimates sufferedfrom difficulties in modeling molecular evolution, due to reliance onfew or misleading fossils or biogeographic events, or limitations of theanalytical techniques available (7, 8). However, these genomic timetrees depended on priors that restricted the maximum age of the tree

based on expert opinion, and changing these priors changed the re-sultant time tree and the rapid radiation of Neoaves relative to the K-Pg event (19, 20).

Interwoven with questions about the temporal history of birds arethose about their biogeographic history; in particular, did Gondwananpaleogeography play a significant role in their early diversification, andwhat historical events were associated with modern birds becomingglobally distributed? With the broad acceptance of plate tectonicsand the rise of phylogenetic thinking, it was proposed that multiplegroups of birds arose on one or more Gondwanan continents (21–23).Although it is now widely acknowledged that some clades of birds,such as Passeriformes, are southern in origin (24, 25), the extensivePaleogene fossil record in the Northern Hemisphere is often inter-preted as being in conflict with the southern origin of many, if notmost, groups (15, 18, 26, 27). Biogeographic history also has importantimplications for the estimation of time trees. For example, the absenceof fossil Neornithes in the Late Cretaceous Niobrara formation ofNorth America has been used to constrain the maximum age of thisclade (4), but if Neornithes originated on a different continent, thiscalibration may underestimate its age.

Here, we present a new estimate of the global avian time tree usingan empirical approach to determine calibration priors. We also tookadvantage of recent advances in our understanding of phylogeneticrelationships among extant (3, 28) and fossil (6, 29, 30) birds and usedslowly evolving nuclear genes amenable to more tractable models ofmolecular evolution (3). The time tree is then used to explore spatialand temporal patterns of global avian diversification.

RESULTS AND DISCUSSION

A new time tree for birdsWe identified avian clades that have a relatively old and well-characterizedfossil whose affinities are well established by phylogenetic analysisand/or derived morphologies. These fossils set a minimum bound forthe stem age of the corresponding clade and its sister group (Fig. 1A)(31–33). However, phylogenetic divergence time estimation also requiresconstraints on the maximum age of clades; otherwise, an arbitrarily oldtree would be compatible with any minimum bound. Maximum age

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constraints can be based on the absence of fossils in earlier fossilif-erous beds, but the absence may reflect fossilization and recovery bi-ases rather than true absence. For example, even if a detailed fossilrecord suggests the absence of a clade in the Paleocene of Europe, theclade may have originated earlier in another less-studied region suchas South America. Fossil recovery biases can be quantified and in-corporated into age estimates (34, 35) but not without theoretical andpractical difficulties (32, 33). This problem is exacerbated by methodsthat constrain clade age based on maximum bounds (36–38) becausebounds do not reflect the uncertainty associated with maximum ageconstraints. A better approach is to use probability density functionsas priors in Bayesian analyses (32, 39), but choosing among differentfunctions and the parameters of those functions has been a subjectiveand contentious issue (33, 40).

Here, we overcame these problems by empirically generating cali-bration priors based on the fossil record. We modeled clade age un-certainty based on distributions of fossils finds. A set of fossil ages t1…tnrepresents a sample from a distribution that has a maximum bound q,which is the age of the clade. The objective is to obtain a probabilitydistribution for the age q. Several methods have been developed toestimate the stratigraphic range of taxa from observed fossil ages eitherby assuming simple distributions of fossil ages (41, 42) or by modelingfossil recovery potentials (34). In the simplest case, when fossil agest1…tn are uniformly distributed, the likelihood of a hypothesizedage q is simply 1/qn for q > tn (41, 43), and in the absence of priorinformation, this likelihood is proportional to the probability of q (43).

An important factor that should be taken into account is the geo-graphic dimension of the fossil record, which includes not only fossil-ization and exhumation biases but also the vagaries of dispersal andcolonization processes. For example, a clade may have a temporallydense fossil record in a region including the oldest fossil of the cladeworldwide; in a naïve assessment, this would suggest that the cladeoriginated shortly before the age of its oldest fossil. However, if theclade originated in a different geographic region, this age estimatewould correspond to the age of dispersion into the region, not theage of the clade. We minimized this problem by analyzing the fossilrecord at a large geographic scale using only the first fossil occurrenceof a clade in each continent. Therefore, for each avian clade with awell-characterized old fossil, we determined the oldest fossil on eachcontinent through bibliographic and database searches and kept onlythose clades whose set of ages do not depart from a uniformdistribution (data set 1; table S1). We then parameterized probabilitydensity functions such that they matched the shape of the likelihoodfunctions (fig. S1) and used them as clade age priors in Bayesiandivergence time estimation (table S1; further details and extensionsare explained in Fig. 1 and Materials and Methods).

We used the empirical priors derived above in Bayesian divergencetime estimation in the program BEAST 2 (44), using a genomic dataset of 1156 clock-like exons for 48 species from Jarvis et al. (3) and a dataset with a much denser taxonomic representation of recombination-activating genes (RAG-1 and RAG-2) for 230 species representing 202families and all avian orders. Both data sets resulted in very similarestimates of the avian time tree. Both placed the most recent commonancestor of extant birds in the early Late Cretaceous, with the genomicdata set resulting in slightly older ages [median, 96.6 Ma; 95% highestposterior density (HPD), 84.2 to 114.3 Ma; Fig. 2A] than the RAGdata set (median, 91.5 Ma; 95% HPD, 79.8 to 106.8 Ma; Fig. 2B).These estimates for the crown age of Neornithes are younger than

0 10 20 30 40 50 60

Millions of years ago

B

C

D

E

Wieslochia

0 10 20 30 40 50 60

Acanthisitti Tyranni Passeri

Wieslochia

Eupasseres

Stem branchCalibration node

A

0 10 20 30 40 50 60

Fig. 1. Example of the method used for generating clade age priorsfrom the fossil record. (A) The fossil Wieslochia weissi from the Oligocene
of Germany shows an apomorphy of the suborder Tyranni: a well-developedtuberculum ligamenti collateralis ventralis. Therefore, Wieslochia sets an ab-solute minimum age for the time of origin (stem age) of the Tyranni, which isthe same as the crown age of Eupasseres. The oldest fossil of the suborderPasseri would also set a minimum age for Eupasseres, but it is younger thanWieslochia. Note that fossils that only show an apomorphy of Eupasseresmay be in the stem branch; for this reason, they are not informative regard-ing the minimum age of crown Eupasseres. (B) The first record of Eupasseres(Tyranni or Passeri) in other continents completes a set of fossil occurrencesof ages t1…tn (see data set 1 for details). (C) This set of ages does not departsignificantly from a uniform distribution (Kolmogorov-Smirnov test, D = 0.25,P = 0.7). Therefore, the likelihood function for the upper bound (q) of auniform distribution [1/(q)n for q > tn] is used to generate a distributionfor the true age of Eupasseres. (D) However, the oldest fossil does not havea precise age estimate but was assigned to a geological time interval thatspans several million years (the same is true for other fossils in the set, buttheir ages do not influence the likelihood). Therefore, pseudosamples of tnare generated by sampling uniformly from the time interval to which theoldest fossil was assigned and used for generating multiple distributionsof clade age. (E) Averaging these pseudoreplicated distributions results ina final distribution, which is then modeled with a standard probability den-sity function that mimics its shape: a log-normal distribution, a log mean of1.7, and a log SD of 0.8. This standard distribution is used as clade age prior inBayesian divergence time estimation.
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Struthio camelusRhea americanaTinamus guttatusNothoprocta

Dromaius novaehollandiaeCasuarius casuarius

Apteryx australis

Megapodius freycinetLeipoa ocellataCrax blumenbachiiGuttera pucheraniCallipepla californicaRollulus rouloulGallus gallusBonasa umbellus

Chauna torquataAnseranas semipalmataDendrocygna arboreaAnser albifronsAnas platyrhynchos

Phoenicopterus ruberTachybaptus ruficollisPodiceps cristatusColumba liviaTreron calvaPterocles personatusMesitornis unicolor

Rhynochetus jubatusEurypyga helias

Phaethon lepturus

Otis tardaTauraco erythrolophus

Coccyzus americanusCentropus phasianinusCoua cristata

Guira guira

Aegotheles insignisHemiprocne mystaceaStreptoprocne zonarisChaetura pelagicaPhaethornis griseogularisFlorisuga mellivoraColibri coruscans

Nyctibius grandisSteatornis caripensis

Podargus strigoidesBatrachostomus septimusEurostopodus macrotisCaprimulgus longirostris

Opisthocomus hoazinPsophia crepitansGrus canadensis

Heliornis fulicaSarothrura insularis

Rallus limicola

Burhinus capensisChionis minorPluvianus aegyptius

Haematopus aterRecurvirostra americana

Charadrius vociferus

Thinocorus orbignyianusRostratula benghalensisJacana jacana

Scolopax rusticola

TurnixStiltia isabella

Catharacta skuaAlca torda

Larus marinus

Gavia immerAptenodytes forsteriSpheniscus humboldtiThalassarche bulleri

Pelecanoides magellaniOceanites oceanicus

Puffinus creatopus

Ciconia abdimiiTheristicus melanopisEgretta tricolorPelecanus erythrorhynchusBalaeniceps rex

Anhinga anhingaPhalacrocorax

Fregata minorSula sula

Cathartes auraSagittarius serpentariusPandion haliaetusElanus caeruleusButeo jamaicensisNinox novaeseelandiaeStrix occidentalisTyto albaPhodilus badius

Leptosomus discolorColius colius

Trogon personatusTockus camurusBuceros bicornisPhoeniculus purpureusUpupa epops

Galbula albirostrisBucco capensis

itrooo amialageMLybius hirsutusTrachyphonus erythrocephalus

Capito nigerSemnornis frantzii

Pteroglossus aracari

Indicator variegatusPicumnus cirratusMelanerpes carolinus

Merops pusillus

Todus angustirostrisMomotus momotaAlcedo leucogasterHalcyon malimbicaChloroceryle americana

Brachypteracias leptosomusCoracias caudata

Cariama cristataMicrastur gilvicollisDaptrius aterFalco peregrinusNestor notabilisCalyptorhynchus funereus

Psittacus erithacusMyiopsitta monachus

Alisterus scapularisAcanthisitta chlorisPitta sordida

Smithornis rufolateralisPsarisomus dalhousiaePhilepitta castanea

Sapayoa aenigma

Piprites chlorisPlatyrinchus coronatus

Rhynchocyclus brevirostris

Onychorhynchus coronatus

Oxyruncus cristatus

Tityra semifasciata

Cotinga cayana

Pipra coronataTyrannus tyrannus

Thamnophilus nigrocinereusTerenura sharpeiMelanopareia torquataConopophaga ardesiacaScytalopus magellanicusGrallaria ruficapilla

Sclerurus mexicanusFormicarius colma

Furnarius rufusMenura novaehollandiaeAtrichornis clamosusClimacteris erythropsPtilonorhynchus violaceus

Malurus melanocephalusMeliphaga analoga

Pardalotus punctatus

Petroica cucullata

Irena cyanogaster

Orthonyx teminckii

Nicator chloris

Mohoua albicilla

Pomatostomus isidorei

Lanius excubitor

Vireo philadelphia

Ptilorrhoa caerulescens

Struthidea cinerea

Daphoenositta chrysoptera

Pachycephala hyperthra

Cyanocitta cristata

Melampitta lugubris

Manucodia atraParadisaea raggiana

Cracticus quoyiArtamus leucorhynchus

Oriolus xanthonotus

Coracina novaehollandiae

Rhipidura hyperthraDicrurus adsimilis

Elminia nigromitratus

Monarcha axillaris

Aegithina tiphiaTelophorus dohertyiPrionops plumatus

Batis mixta

Vanga curvirostris

Philesturnus carunculatus

Chaetops frenatusPicathartes gymnocephalus

Bombycilla garrulus

Cinclus cinclusCatharus ustulatusMuscicapa ferruginea

Sturnus vulgarisMimus patagonicus

Sitta carolinensisCerthia familiarisTroglodytes aedon

Remiz pendulinusParus major

Aegithalos iouschensisHirundo rustica

Regulus calendula

Acrocephalus newtoni

Megalurus palustrisSphenoeacus afer

Pycnonotus barbatus

Cisticola anonymus

Zosterops senegalensis

Sylvia nana

Alauda arvensis

Promerops cafer

Dicaeum aeneum

Nectarinia olivacea

Melanocharis nigra

Paramythia montium

Prunella collarisPloceus cucullatus

Passer montanusMotacilla cinerea

Taeniopygia guttata

Fringilla montifringillaCalcarius lapponicusEmberiza schoeniclusThraupis cyanocephala

100 90 80 70 60 50 40 30 20 10 0

MioceneOligoceneEocenePaleoceneLate PSPO

QNeogenePaleogeneCretaceous

AcanthisittiEurylaimides

Psittaciformes

Passeriform

es

TyranniP

asseridaC

orvida

FalconiformesCariamiformes

Bucerotiformes TrogoniformesLeptosomatiformesColiiformesStrigiformes

Accipitriformes

ProcellariiformesSphenisciformes

GaviiformesPhaethontimorphae

Charadriiformes

Coraciiformes

Piciformes

Gruiformes

Opisthocomiformes

Caprimulgiformes

Cuculiformes OtidiformesMusophagiformes

ColumbimorphaePhoenicopterimorphae

Galliformes

AnseriformesCasuariiformes

Struthioniformes

ApterygiformesTinamiformesRheiformes

Tyrannides

Furnariides

Menuroidea

Meliphagoidea

Passeroidea

Muscicapoidea

Certhioidea

Sylvioidea

Corvoidea

Petroicidae

Orthonychidae

Paroidea

Bombycilloidea

Pelecaniformes

Aequornithia


Neoaves 69.0

53.0

Galloanseres 72.5

Palaeognathae 65.3

Neognathae 85.1

91.5

60.5

B

80 60 40 20 0


100 80 60 40 20 0

Tinamus guttatusStruthio camelusAnas platyrhynchosGallus gallusMeleagris gallopavoPhoenicopterus ruberPodiceps cristatusColumba liviaMesitornis unicolorPterocles gutturalisCuculus canorusChlamydotis macqueeniiTauraco erythrolophusAntrostomus carolinensisChaetura pelagicaCalypte annaOpisthocomus hoazinCharadrius vociferusBalearica regulorumPhaethon lepturusEurypyga heliasGavia stellataFulmarus glacialisPygoscelis adeliaeAptenodytes forsteriPhalacrocorax carboNipponia nipponPelecanus crispusEgretta garzettaCathartes auraHaliaeetus albicillaHaliaeetus leucocephalusTyto albaColius striatusLeptosomus discolorApaloderma vittatumBuceros rhinocerosPicoides pubescensMerops nubicusCariama cristataFalco peregrinusNestor notabilisMelopsittacus undulatusAcanthisitta chlorisManacus vitellinusCorvus brachyrhynchosTaeniopygia guttataGeospiza fortis


A

Fig. 2. Time trees of modern birds from Bayesian divergence time estimation using fossil calibrations.Maximum clade credibility (MCC) trees froma Bayesian divergence time estimation using calibration priors inferred from the fossil record. (A) MCC tree from the analysis of 124,196 bases from the first
and second codon positions of 1156 clock-like genes from Jarvis et al. (3) and 10 calibration priors. (B) MCC tree from the analysis of 4092 bases of therecombination-activating genes for 230 species and 24 calibration priors. Black diamonds are calibration nodes, black dots are clades that were con-strained to match relationships supported by recent multilocus and genomic analyses (3, 28), red density distributions are clade age prior probabilitiesderived empirically from a quantitative analysis of the fossil record of clades, and blue bars represent 95% highest posterior densities for node age fromthe posterior distribution. Median ages are indicated for large clades mentioned in the text (blue dots).
Claramunt and Cracraft Sci. Adv. 2015;1:e1501005 11 December 2015 3 of 13


most previous estimates (5, 10–12), but higher posterior densitiesoverlap with the recent analysis of bird genomes (3), in which a maxi-mum age constraint was assumed for the age of Neornithes at the Early-Late Cretaceous boundary. Our analysis recovered a relatively youngage for Neornithes without prior constraints on its age.

Radiation within the three major clades—Palaeognathae, Galloan-seres, and Neoaves—began around the K-Pg transition (Fig. 2). Initialcladogenesis in Galloanseres and Neoaves occurred just before theK-Pg transition, whereas the timing of initial cladogenesis in Palaeog-nathae is poorly constrained and spans pre– and post–K-Pg times(Fig. 2). Overall, it is possible that initial radiation of these three majorcrown clades occurred more or less simultaneously around (and prob-ably before) the K-Pg event, thus suggesting common causal factors.All avian orders originated during the Paleocene (median stem age;Fig. 2), except for Anseriformes and Galliformes, which originatedin the latest Cretaceous, and some orders within the higher ratites,which may have originated in the late Paleocene or early Eocene, tak-ing into account uncertainty.

Large-scale biogeographic history of birdsNext, we integrate phylogenetic relationships and the avian time treewith the spatial history of the major lineages of birds, set in the contextof paleogeography and paleoclimatology. Because biogeographic his-tory is far too complex to be inferred from ancestral reconstructionsalone, our interpretations of the spatial history of birds are also derivedfrom the joint geographic and temporal history among deep stemlineages (that is, avifaunas), the fossil record, phylogenetic and bio-geographic patterns within clades, and how those data can be reconciledwith Earth history.

We identified the geographic origin of Neornithes and of its threemajor subclades (Palaeognathae, Galloanseres, and Neoaves) to beWest Gondwana, here taken to encompass a united continental SouthAmerica, West Antarctica, and portions of East Antarctica (Fig. 3). Thisconclusion is robust to methodological assumptions (parsimony versusprobabilistic modeling) and alternative tree topologies, with the ex-ception that the likelihood reconstruction for the most recent commonancestor of Palaeognathae is ambiguous and includes bothWest Gond-wana and the Palearctic (fig. S3). In addition to these basal groups, wereconstructed 22 major groups of Neornithes as being present in SouthAmerica by the end of the middle Paleocene (~59.2Ma) (Fig. 3 and tableS2). Because of its taxonomic composition, this avifauna likely repre-sented a broad sample of morphological and ecological diversity, fromterrestrial lineages (ratites and stem-Gruiformes), freshwater and marine(stem-Charadriiformes, Sphenisciformes, Procellariiformes, and Phoeni-copteriformes), predators (Cariamiformes and Falconiformes), nocturnaland aerial specialists (Caprimulgiformes), and arboreal groups (Coracii-morphae, Psittaciformes, andPasseriformes).The estimatedmeanages in-dicate that this diverse assemblage was present very soon after the K-Pg,but uncertainties inherent in dating do not rule out the existence ofsome Neoavian lineages in the latest Cretaceous. The Paleocene avianradiation in South America was paralleled by a buildup of eutherianmammal diversity (45). West Gondwana would have been a large land-mass in the latest Cretaceous and Paleocene, with predominantly warm,moist, equable climates (46) that would have facilitated the accumula-tion of diversity within a variety of environments, with a modern rain-forest being establishedover a large portion of SouthAmerica (45, 47, 48),and with warm to cool subtropical/temperate forests in the far south onAntarctica (46, 49).


We hypothesize that Neornithes spread from West Gondwana tothe rest of the world via two principal routes. The first route is a trans-Antarctic corridor that linkedWest Gondwana to Australia and Zealandiaduring the Cretaceous and early Paleogene (Fig. 3) (44). This corridorenabled the establishment of a widespread southern biota with a diver-sity of organisms, including plants (50), dinosaurs (51), mammals (52),and birds (Fig. 3 and table S2). The exact configuration of the land con-nection between South America and West Antarctica is uncertain, butthis terrestrial corridor was potentially disrupted as early as ~50 Ma toas late as ~40 to 37 Ma, when a deep opening of the Drake Passage isinferred (53–56). Continental blocks comprising the corridor wouldhave remained in proximity until ~30 Ma (55, 57).

Before ~83 Ma, Zealandia was conjugate to the eastern Australianmargin and to West Antarctica in the south (58, 59). At that time, sea-floor spreading began in the Tasman Basin and south of the CampbellPlateau, severing a direct connection between Zealandia and WestAntarctica, thus establishing the Tasman Gateway as the primary cor-ridor for a K-Pg biota to enter Australia and then Zealandia (59). TheSouth Tasman Rise did not rift from East Antarctica until the middleto late Eocene ~40 to 33 Ma; before then, the continental fragmentscomprising the South Tasman Rise were intermittently subaerial andshallow marine, with terrigenous sedimentation persisting through theEocene (60, 61). Our results suggest that at least seven to nine majorclades involving palaeognaths, Galloanseres, caprimulgiforms, andpsittacopasseres (parrots and passerines) were shared with Australiabefore its separation from Antarctica (table S2). Two additional line-ages, tree swifts (Hemiprocnidae; 95% HPD, 21.4 to 43.1 Ma) and theKagu (Rhynochetidae) (95% HPD, 16.9 to 45.2 Ma), may have alsobeen part of this interchange, considering age uncertainties. Previously,biogeographers had assumed that the ~83-Ma split between Zealandiaand West Antarctica and the initial formation of the Tasman Seaimplied that younger elements of the biota must have arisen vialong-distance dispersal (23), but this assumption of a deep age for theZealandia biota is no longer necessary (59). Rather, biogeographicpatterns of deeper avian lineages were likely established by multiple epi-sodes of vicariance within an early Tertiary biota that occupied Australiaand emergent portions of Zealandia (table S2). The presence in Zealandiaof two ancient lineages of flightless palaeognaths (kiwis and moas) [theflightless Kagu on New Caledonia and its flightless sister group(Aptornis) on New Zealand], as well as ancient lineages of parrotsand passerines, is consistent with this interpretation.

We propose that there was a second Paleogene gateway for avifaunalexpansion out of West Gondwana involving North America (heretermed the North American Gateway hypothesis). Although it has longbeen assumed that there was a wide ocean barrier between South andMiddle America through the Late Cretaceous and Paleogene until thePlio-Pleistocene, we hypothesize a northward avifaunal expansion atthis time coincident with the first appearances of Laurasian metatherianand placental mammals in South America (45, 62), thus implying thepresence of a land bridge. Although the paleogeographic setting of lowerMiddle America is complex and controversial, this interpretation is con-sistent with a growing number of tectonic models that posit a southernland bridge (63–65) that resulted from subduction, arc magnetism, andcollisionary processes involving movement of the Galapagos large igneousprovince into the Caribbean, spanning K-Pg times.

Our results suggest a central role for North America as a gatewayfor biotic dispersion into the Holarctic, especially during the Paleoceneto early/middle Eocene. Northern Hemisphere Paleogene environments

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Muscicapoidea

Certhioidea

Bombycilloidea

DinornithiformesTinamiformes

Apterygiformes

Rheiformes

Eurylaimides

AcanthisittidaePsittaciformes

Falconiformes

TyrannidesTT

Furnariides

MenuroideaMeliphagoidea

Passeroidea

Sylvioidea

Corvoidea

Petroicidae

Orthonychidae

Paroidea

Phoenicopterimorphae

Cariamiformes

BucerotiformesTrogoniformesLeptosomiformesColiiformesStrigiformes

Accipitriformes

Procellariiformes

SphenisciformesGaviiformesPhaethontimorphae

Charadriiformes

Coraciiformes

Piciformes

Gruiformes

Opisthocomiformes

Caprimulgiformes

Cuculiformes Otidiformes

MusophagiformesColumbimorphae

Galliformes

Anseriformes

Casuariiformes

Struthioniformes

Pelecaniformes

Passeriform

es

TyranniTT

Passerides

Corvides

Coraciornithia


MioceneOligoceneEocenePaleoceneLate PlePliQ.NeogenePaleogeneCretaceous

90 80 70 60 50 40 30 20 10 0

Aequornithia

Zealandia

PalearcticNearctic

Australia

South America

Indomalay

Afrotropical

Madagascan

Fig. 3. Time tree of modern birds with reconstruction of ancestral geographic regions. Fitch parsimony optimizations of ancestral geographic regionsare shown at the nodes. Multiple regions at a node represent alternative, equally parsimonious optimizations. The tree is the maximum clade credibility tree
of a Bayesian analysis of recombination-activating genes for 230 species and 24 calibration priors and with the addition a posteriori of 25 fossil taxa thatrepresent Holarctic distributions for clades now restricted to the tropics. Distributions at the tips are those of the clades they represent. Schematic representationsof global paleogeography at the K-Pg transition, the middle Eocene, and the middle Miocene are shown together with major postulated interregional connectionsas inferred from paleogeographic evidence and biogeographic analysis. Higher-level taxa are indicated on the right (see fig. S2 for species names).
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were broadly tropical and subtropical at lower latitudes and subtropical-warm temperate at higher latitudes, especially toward the Paleocene-EoceneThermal Maximum (66–69). We infer that these avifaunas diversifiedwithin the Nearctic and spread into the Palearctic by the end of thePaleocene and earliest Eocene ~56 to 53 Ma (Fig. 3 and table S2).

The biogeographic analyses suggest that North America played aformative role in the origins of lineages that subsequently diversified inthe Old World. Thus, the Green River Formation (53 to 51 Ma) (70) inNorth America and the Fur Formation (55 to 54 Ma) (71) and Messeloil shales (47 Ma) (29) in Europe record many of the stem lineages thatwere elements of a widely distributed Paleogene avifauna (table S2). Thetime tree is consistent with these lineages having initiated diversificationbefore deposition of these fossils. For example, instead of the Coracii-morphae arising in Africa (72), our optimizations indicate that Lepto-somatiformes, Coliiformes, and Coraciiformes colonized the Paleotropicsindependently from North American ancestors (Fig. 3). Given the pres-ence of many of these lineages in the early Paleogene of Europe, we inferthat they reached the western Palearctic through a North Atlantic corri-dor before ~52 Ma (table S2). The tectonic history of the North Atlanticin the Paleogene indicates land connections among northeastern NorthAmerica, Greenland, and Europe (73, 74), and paleontological evidencerecords mammalian faunal interchange until sometime in the earlyEocene (68, 75), when sea-floor spreading between northeastern Green-land and Europe would have created an ocean barrier ~53 to 52Ma (73, 76).

Expansion into other Old World landmasses is more difficult tocircumscribe temporally and geographically. The avian Paleogene re-cord for Africa is sparse, and that for Madagascar is lacking entirely(29). Some old stem clades now characteristic of these two land massesare found in the North American or European fossil record (29). BothMalagasy endemic cuckoo rollers (Leptosomatiformes) and true rollers(Coracioidea) have Holarctic Paleogene records, but when they didarrive in Africa or Madagascar is unclear. Our reconstructions suggestthat lineages arrived in Madagascar in the Paleocene (mesites, Mesit-ornithidae), the Eocene (ground rollers, Brachypteraciidae), and theOligocene (vangas, Vangidae; Fig. 3), suggesting that the buildup ofthe Malagasy endemic avifauna may have been a protracted processthat spanned at least the entire Paleogene.

A second route from North America to the Old World—the Beringland bridge—would have been emergent over much of the Tertiary and,depending on eustatic sea levels and high-latitude temperature gradi-ents, would have facilitated frequent biotic interchange between Asiaand North America (77, 78). However, a Beringian corridor for Paleo-gene avifaunas is not evident in our analysis, partly as a result of a poorfossil record in northern Asia. Cranes and their allies (Gruiformes) pro-vide an exception, with Eocene-Oligocene fossil families Geranoididaein North America and Eogruidae in Asia showing close affinities (29).Several other stem lineages associated with the North Atlantic corridormay also have had Paleogene histories across Beringia, including stem-Struthioniformes (ostriches) and Caprimulgiformes such as frogmouths(Podargidae) and swifts (Apodidae) (Supplementary Materials).

A novel implication of the North American Gateway hypothesis isthat the roots of the “Old World” suboscines (Eurylaimides) are in theNew World. Four well-supported lineages are known, but their inter-relationships are uncertain (79, 80). One of these lineages is Sapayoaaenigma of the rainforests of eastern Panama and northwestern Colombia.The other three lineages are tropical African–Southeast Asian lineages,with a few young species reaching Australasia. We estimate the crownradiation of Eurylaimides to be ~37 Ma; thus, biogeography and age


suggest that one lineage or possibly two lineages independently colo-nized the Old World, with Sapayoa being relictual. If our estimate forthe age of crown Eurylaimides at ~37 Ma is correct, then it impliesthat these lineages entered the paleotropics via Beringia, not acrossthe North Atlantic.

A key event in avian evolution was the diversification of songbirds(Passeri). Our reconstructions indicate that dispersion into East Gondwanaof the Acanthisitti probably occurred independently of Passeri (25, 81)(Fig. 3), and we place the most recent common ancestor of the latter onthe Australian landmass at 47.3Ma (HPD, 43.1 to 51.6), which is youn-ger than current estimates (24, 82, 83). Over the next 5 to 7 Ma, oscinesunderwent substantial phenotypic and ecological evolution in greaterAustralia; by ~40 Ma, this had resulted in the endemic corvidan radia-tion and early lineages that reached Zealandia (Fig. 3). Contemporane-ously, oscine lineages were transferred fromAustralia to Southeast Asiaand Africa, including the Eupetidae (40.6 Ma) and the Promeropidae(39.5 Ma), the sister group of the Laurasian Passerides (Fig. 3). Theselineages mark the beginnings of the great passeridan radiation acrossthe paleotropics, Eurasia, and eventually theNewWorld (25). This earlyAustralian-Asian exchange also involved lineages of corvidans, includingat least stem-vireonids (34.6 Ma), campephagids (34.4 Ma), and pachy-cephalids (31.7 Ma). These ages are coincident in time with the earlynorthward drift of Australia and are estimates of the origin of stemlineages, not of crown clades, which are younger (for example, thecrown age for Eupetidae is 26.8 Ma). By the early Oligocene (around33.9 Ma), portions of northwestern continental Australia were adjacentto Asia, and collision followed in the Miocene (84, 85). In addition, theMiocene-Pliocene left-lateral motion along the Sorong Fault transport-ed continental slivers to the west toward Asia. Thus, hypotheses oflong-distance dispersal across wide ocean gaps (83, 86) may not benecessary to explain this complex avifaunal interchange. Once intropical Asia by the late Eocene, each of the major songbird lineagesradiated extensively into the Oligocene and early Miocene environ-ments of the Afrotropics and Eurasia (Fig. 3) (25, 83, 86). Many lineagesthen enteredNorth America at various times across an emergent Beringland bridge (25).

Temporal dynamics of avian diversificationTo explore the effects of Earth history on avian diversification dynamics,we analyzed changes in diversification rates through time. We foundthat net diversification rates (speciation − extinction) track changes inglobal climate over the entire timespan of modern bird evolution: ratesincrease during periods of climate cooling and decrease during periods ofclimate warming (Fig. 4A). Relative extinction (extinction/speciation)was low, and periods of increased extinction coincide with periods ofhigh net diversification (Fig. 4B), suggesting that the overall dynamics isdominated by changes in rates of speciation. Environment-dependentbirth-death likelihood models, in which diversification rates arefunctions of a time-dependent environmental variable (87), also indicatethat rates of speciation and extinction are negatively correlated withglobal temperature (table S3).

We propose that this macroevolutionary dynamics is largely theresult of climate change inducing biome fragmentation and vicariance(that is, climate-induced vicariance). During major cooling trends ofthe Late Cretaceous (88) and the Cenozoic (89), tropical biomes wouldhave experienced successive waves of retraction and fragmentation(49, 66, 67), which resulted in population fragmentation and increasedrisk of extinction across entire faunas, but also increased chances of

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speciation among the newly isolated populations (90). Thus, providedthat speciation rates were higher than extinction rates, this scenarioresults in higher net diversification of entire avifaunas during periodsof climate deterioration. Conversely, expansion of thermophilic forestsduring warm periods (49, 66, 67) promoted connectivity and homog-enization of avifaunas (also suggested by a wave of worldwide disper-sion; Fig. 3), a phenomenon also documented among austral fossilfloras (91) and boreal mammalian faunas (68, 75). The final burstof diversification in our analysis occurred soon after the middle Miocenecooling episode, which is associated with global retraction of tropical andmesic biomes and expansion of steppes and deserts (92–95). Therefore,the middle Miocene cooling may have fragmented distributions andincreased diversification of not only humid tropical but also subtropicaland mesic taxa.

Although climate-induced vicariance predicts a final major burst ofdiversification during Pleistocene glaciations, this burst cannot be de-tected in our time tree because of sampling (that is, there are no branch-ing events in the last 10 Ma). That most avian time trees showslowdowns in diversification toward the present (95) seems to falsifythis prediction, but apparent slowdowns are likely to be artifacts ofnucleotide model misspecification (96), deep gene-tree coalescence(97), and incomplete species sampling (98). Alternatively, climate-induced vicariance can also be compatible with low diversificationduring the Pleistocene if extinction rates increased more than speciationrates, thus dampening net diversification. Complete and calibratedspecies trees are needed to resolve this matter.

Other events in Earth history may also have influenced diversifica-tion rates in Neornithes. In particular, the rate increase at the end of


the Cretaceous occurred near the K-Pg transition, suggesting a possi-ble association with the K-Pg extinction event. Although the rate in-crease started before the K-Pg transition, coinciding with the latestCretaceous cooling trend, the magnitude of the rate increase suggestsa role for the K-Pg event in increasing rates further. The extent of thiseffect and its particular mechanisms requires further investigation. Al-though the K-Pg event marked the extinction of close relatives such asEnantiornithes and basal Ornithurae, the extent to which it affectedmodern birds directly is unclear from the fossil record because of thescarcity of Neornithes remains before and after the event (6, 17, 29, 96).Our biogeographic reconstructions suggest that Neornithes occupiedWest Gondwanan continents during the K-Pg transition and, therefore,like other animals and plants (91, 97, 98), may have escaped the cata-strophic effects of the impact. On the other hand, if multiple earlylineages of Neornithes faced extinction during the K-Pg event, thatmay have created a false signal of rate increase in the reconstructed phy-logenies, in which case the apparent increase is merely a consequence ofmissing lineages before the event (99, 100). Finally, the big-bang modelposits that surviving lineages of Neornithes would have experienced ec-ological opportunity that may have stimulated diversification (15, 18).In any case, catastrophic extinction events may not be general drivers ofdiversification in modern birds because they cannot explain changes indiversification rates over most of the Cenozoic (fig. S4). Thus, there areno major meteorite impacts, volcanism, or mass extinctions in the Mi-ocene, when diversification rates increased dramatically (Fig. 4A and fig.S4). Our data suggest, in contrast, that global changes in climate arecorrelated with changes in diversification rates throughout the entirehistory of modern birds. Statistical comparison of diversification models

A

B

wo

Fig. 4. Diversification rates through time for modern birds and major events in Earth history during the Late Cretaceous and the Cenozoic.(A) Red: Net lineage diversification rate (speciation-extinction) estimated for 5-Ma intervals using birth-death shifts models (120) (lines are medians of 500
estimates from a sample of the posterior distribution of trees from the Bayesian time-tree analysis; light boxes around medians are interquartile ranges).Blue: Deep-ocean temperatures estimated from a global compilation of benthic foraminifera oxygen isotope data (124) represented by a local regressionsmoother and associated 95% confidence intervals. Major tectonic and meteorite events are also indicated. (B) Relative extinction rate (extinction/speciation) (lines are medians, and light boxes around medians are interquartile ranges from 500 estimates from the tree posterior).
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also favors climate over extinction events as drivers of avian diversification(Supplementary Materials). Ultimately, we cannot reject a potential effectof the K-Pg mass extinction event on modern bird diversification, butfurther research on this matter should consider the potentially pervasivebackground effect of climate-induced vicariance on diversification.

Climate-induced vicariance may have a prominent role in control-ling macroevolutionary rates (90), but it may be difficult to detect inpaleontological data sets. Actually, except for a clear signal of mass ex-tinctions associated with catastrophic events, general drivers of temporalmacroevolutionary dynamics in terrestrial tetrapods have been difficultto identify (87, 101–103). Climate-induced vicariance may be obscuredin paleontological data sets because it results in speciation in fragmentedpopulations that are difficult to detect in a geographically sparse fossilrecord (104). Conversely, during benign climates, populations expandand have higher chances of being detected, resulting in a bias in whichnew species remain undetected until they expand during warmperiods. This hinders the detection of climate-induced vicarianceand creates a false signal of positive associations between diversificationand warming in the fossil record.

Climate-induced vicariance has received considerable attentionin microevolutionary studies of diversification. There is now wide-spread evidence of population differentiation and speciation associ-ated with habitat fragmentation and biogeographic refugia (105–110).Climate-induced vicariance also explains how niche conservatismmight stimulate speciation (111). Finally, analyses of geographic varia-tion in diversification rates among extant birds also suggest higher spe-ciation and extinction rates in regions with harsher climates (14, 112, 113).Therefore, climate-induced vicariancemay explain avian diversificationthrough space and time, providing a unified framework for understand-ing large-scale biodiversity dynamics in birds.

CONCLUSIONS

We generated a new time tree for modern birds that revealed strikingpatterns of their evolutionary history. We found that modern birdsoriginated in the early Late Cretaceous in Western Gondwanan con-tinents but did not diversify much until the K-Pg transition. This,combined with the poor overall quality of the Late Cretaceous avianfossil record (96), explains in part the scarcity of fossils of modernbirds in the Cretaceous, thus partially resolving the “clocks versusrocks” controversy. Modern birds expanded from West Gondwanato the rest of the world through two routes. One route was a trans-Antarctic interchange during the Paleogene that resulted in the presenceof multiple avian groups in Australia and Zealandia. The other routewas a North American Gateway, facilitated by an inter-American landbridge during the Paleocene that allowed expansion and diversificationof modern birds into the Holarctic and eventually the Paleotropics. TheNorth American Gateway hypothesis explains the presence of numer-ous neoavian groups in the Eocene of North America and Europe with-out the need to postulate northern origins for these groups or to rejectthe importance of Gondwana in early avian evolution.

The new time tree also reveals a striking pattern in which avian netdiversification rates increased during periods of global climatic deteri-oration. This pattern is consistent with a model of climate-inducedvicariance in which biome fragmentation triggers speciation pulsesacross entire avifaunas. Thus, initial rapid radiation of Palaeognathae,Galloanseres, and especially Neoaves can be explained by the Late


Cretaceous cooling trend, with perhaps additional effects of the K-Pgmass extinction. Overall, the new time tree reveals that the historicalbiogeography and diversification dynamics of modern birds was tightlylinked to the paleogeographic and climatic history of planet Earth.

MATERIALS AND METHODS

Estimation of clade age from the fossil recordIf fossil occurrences belonging to a clade are uniformly distributed be-tween the present and the time of origin of the clade q, the likelihoodof a hypothesized age q given the observed fossil age occurrences t1…tnis simply 1/qn for times older than the oldest fossil tn (41, 43). Thislikelihood is proportional to the probability density of q in the absenceof prior information (43). Instead of using the present as the baseline,the age of the most recent fossil can be used as the baseline, in whichcase the likelihood becomes 1/(q − t1)

n − 1 for q > tn (42). Therefore,the likelihood depends on the age of the oldest fossil tn, the number offossil occurrences n, and the timespan encompassing those occurrences (q− t1). The higher the number of fossil occurrences n and the narrowerthe timespan between the youngest fossil and clade age, the higher theconcentration of the likelihood near the oldest fossil tn. Then, a prob-ability density function is parameterized in a way that replicates theshape of the likelihood. This probability density function can be im-plemented as a clade age prior in molecular Bayesian divergence timeestimation. We also considered the case in which fossil ages have un-certainty, specifically when the oldest or youngest fossils are assignedto a geological time interval that spans more than 1 Ma. In such cases,we uniformly sampled pseudoreplicated sets of fossil ages from thetime interval, estimated likelihood distributions for clade age, andcomputed an average probability distribution across pseudoreplicates.The methodology is explained with an example in Fig. 1. Functions forgenerating empirical calibration priors from the fossil record in the Rlanguage are available at https://github.com/evolucionario/cladeage.

Phylogenetic time-tree analysisWeconducted aBayesian time-tree estimation in the programBEAST2(44) using two molecular data sets: one that emphasizes genomic cover-age and another that emphasizes taxonomic coverage. The genome-scaledata set consisted of the first and second codon positions of 1156 clock-like exons for 48 species from Jarvis et al. (3), whichwe filtered formissingdata (positions with missing data or gaps for any taxa were deleted), andresulted in a final alignment of 124,196bases. Tomaximize taxonomic cov-erage, we used sequences of the slowly evolving recombination-activatinggenes (RAG-1 and RAG-2) for 230 species representing 202 familiesand all avian orders (alignment length, 4092 bases). Amplification andsequencing protocols for new RAG sequences followed previous studiesof avian RAGs (25). For the RAG alignment, we determined an optimalsubstitution model and partitioning scheme simultaneously using thePartitionFinder algorithm (114). The genomic data set was analyzedunder a single GTR+ gamma substitutionmodel. Bayesian inference wasperformed using BEAST 2 (44). Rate heterogeneity across lineages wasmodeled with a relaxed lognormal clock (39). Priors on rates of substi-tution and clocks were set to defaults (as in Beauti 2.1).We ran analysesusing a birth-death tree prior with incomplete sampling that takes intoaccount the fact that we sampled a small fraction of all avian diversity(Supplementary Materials). Priors on calibration clades were setusing exponential or log-normal functions, with parameters chosen as

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to mimic the empirical density distributions for the origin of clades (fig.S1 and table S1).We ran analyses without sequence data to evaluate thebehavior of calibration priors (115). The tree topology of the RAG dataset was estimated togetherwith divergence times, except for some clades(Fig. 2B) that were constrained to match relationships supported by re-cent multilocus and genomic analyses (3, 28). The tree of the genomicanalysis was fixed to the ExaML Total Evidence Nucleotide Treetopology of Jarvis et al. (3). Posterior samples were obtained from sixindependentMarkov chainMonte Carlo runs of 80million generations,each ofwhich sampled every 8000 generations for the RAGdata set, andfrom four runs of 60 million generations sampled every 6000 genera-tions for the genomic data set. Adequacy of sampling and convergencewas evaluated by examining the traces and effective sample sizes of like-lihoods and parameters.

Ancestral area reconstructionWe divided the globe into eight regions that reflect both current globaldistributional patterns and major continental plates to ensure that areadefinitions are meaningful throughout the Cenozoic (SupplementaryMaterials). We assigned regions to the tips of the tree based on thecurrent distribution of the clades they represent (data set 2). Regionswere coded as different states of a single character, and clades distributedacross multiple regions were treated as “polymorphic.”We reconstructedancestral areas using Fitch parsimony, a nonparametric method thatimplies an island model (116). This method assumes geographic transi-tions rather than agglomeration of ancestral areas and is appropriatewhen transitions are rare (116, 117)—two conditions that may be moreappropriate for large biogeographic regions because most avian speciesare restricted to single continents among which dispersal events are rare.In addition, more complex methods require complete phylogenies inwhich the tips of the tree are individual lineages (116, 118). In the presentcase, because the tips of the tree are solely representatives of clades, someof which are large, statistical methods may result in biased parameter es-timates, compromising ancestral area estimation. Parsimony optimiza-tions were obtained using the function ancestral.pars in the phangornlibrary (119) with the option MPR to obtain all possible parsimony re-constructions. Nevertheless, to explore the effect of methodological as-sumptions, we also used a probabilistic dispersal-vicariance likelihoodmodel implemented in the library BioGeoBEARS in R (118) (Supple-mentary Materials). We also explored the effect of using an alternativetree topology (4) (Supplementary Materials). The fossil record indi-cates that many taxa, which are today restricted to tropical latitudes,were once present in the northern continents (29); therefore, includingonly extant taxa can bias ancestral reconstructions toward tropicalareas. To minimize this bias, we added 25 fossil taxa to the tree repre-senting Holarctic distributions for clades now restricted to the tropics(data set 2). Fossil taxa were attached at the midpoint between theirage and the stem age of the clade to which they belong, using a new Rfunction (available at https://github.com/evolucionario/fossilgraft),and treated as terminals in biogeographic reconstructions.

Diversification dynamics analysisTo analyze variation in diversification rates through time, we esti-mated rates for 5-Ma intervals using the results of the RAG data setand the function bd.ME.optim in the TreePar library (120). We ana-lytically accounted for missing taxa using the option “groups” (121) inwhich we specified the actual number of species in taxa represented byeach terminal of the tree; the richness of each terminal taxon was es-


timated using current taxonomic knowledge (122, 123) and can befound in data set 2. We also fitted environment-dependent birth-deathmodels in which diversification rates are functions of a time-dependent environmental variable (87): we modeled different scenariosin which speciation or extinction rates vary through time as functions ofchanges in paleotemperatures. Deep-sea paleotemperatures werederived from a global compilation of benthic foraminifera oxygen iso-tope (d18O) data (124) and new estimating equations (125). Rate de-pendency on global temperature could be linear [r(t) = r0 + aT(t)] orexponential [r(t) = r0eaT(t), in which r0 and a are estimated parametersand T(t) is a function that describes changes in temperature over time,in this case, a smooth-spline function with 50 degrees of freedom ofdeep-ocean temperature data].

SUPPLEMENTARY MATERIALSSupplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/11/e1501005/DC1TextFig. S1. Probability density distributions for the age of the most recent common ancestor(crown age) of 24 avian clades in the RAG data set inferred from the distribution of fossiloccurrences.Fig. S2. Biogeographic ancestral area reconstruction using Fitch parsimony optimization.Fig. S3. Alternative biogeographic ancestral area reconstructions.Fig. S4. Diversification through time of modern birds and Earth history events.Fig. S5. Effect of the tree prior on Bayesian divergence time estimation.Table S1. Probability distributions of clade age from fossil occurrences, used as calibrationpriors in Bayesian divergence time analysis in BEAST 2.Table S2. Reconstructions of the taxonomic composition of Late Cretaceous–Cenozoic globalavifaunas.Table S3. Environmental birth-death models of the associations between diversification ratesand global temperature in modern birds.Table S4. Birth-death shift models representing associations between Earth history events anddiversification rates in modern birds.Data set 1. Fossils used for calibration.Data set 2. Biogeographic and richness information.References (126–185)

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Acknowledgments: We thank the Burke Museum for providing important tissue samples,G. F. Barrowclough for sharing DNA extractions and sequences, and W. M. Mauck and J. McKay forgenerating additional DNA sequences. We thank B. T. Smith and R. MacPhee for comments on anearly version of the manuscript and two anonymous reviewers for comments on the submittedversion. Funding: This work was supported by the F. M. Chapman Fund (American Museum ofNatural History) and the U.S. National Science Foundation (awards 1241066 and 1146423 to J.C.).Author contributions: S.C. and J.C. conceived the study. S.C. devised and implemented the cladeage prior estimation method and diversification analyses, and compiled the fossil, richness, andbiogeographic data sets. S.C. and J.C. designed and conducted the time-tree analyses and bio-


geographic reconstructions. S.C. and J.C. wrote the manuscript. Competing interests: The authorsdeclare that they have no competing interests. Data and materials availability: All data neededto evaluate the conclusions in the paper are present in the paper and/or the SupplementaryMaterials. Additional data related to this paper may be requested from the authors. New se-quences were deposited in GenBank (KT954347 to KT954541), whereas alignments and maximumclade credibility trees were deposited in TreeBASE (http://treebase.org; submission 17445). Data-bases of fossils used for calibration (data set 1) and the biogeographic and species richness data(data set 2) are available as online supplementary materials.

Submitted 29 July 2015Accepted 2 November 2015Published 11 December 201510.1126/sciadv.1501005

Citation: S. Claramunt, J. Cracraft, A new time tree reveals Earth history’s imprint on theevolution of modern birds. Sci. Adv. 1, e1501005 (2015).

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http://treebase.org

advances.sciencemag.org/cgi/content/full/1/11/e1501005/DC1

Supplementary Materials for

A new time tree reveals Earth history’s imprint on the evolution of

modern birds

Santiago Claramunt and Joel Cracraft

Published 11 December 2015, Sci. Adv. 1, e1501005 (2015)

DOI: 10.1126/sciadv.1501005

This PDF file includes:

Text

Fig. S1. Probability density distributions for the age of the most recent common

ancestor (crown age) of 24 avian clades in the RAG data set inferred from the

distribution of fossil occurrences.

Fig. S2. Biogeographic ancestral area reconstruction using Fitch parsimony

optimization.

Fig. S3. Alternative biogeographic ancestral area reconstructions.

Fig. S4. Diversification through time of modern birds and Earth history events.

Fig. S5. Effect of the tree prior on Bayesian divergence time estimation.

Table S1. Probability distributions of clade age from fossil occurrences, used as

calibration priors in Bayesian divergence time analysis in BEAST 2.

Table S2. Reconstructions of the taxonomic composition of Late Cretaceous–

Cenozoic global avifaunas.

Table S3. Environmental birth-death models of the associations between

diversification rates and global temperature in modern birds.

Table S4. Birth-death shift models representing associations between Earth

history events and diversification rates in modern birds.

References (126–186)

Other Supplementary Material for this manuscript includes the following:

(available at advances.sciencemag.org/cgi/content/full/1/11/e1501005/DC1)

Data set 1 (Microsoft Excel format). Fossils used for calibration.

Data set 2 (Microsoft Excel format). Biogeographic and richness information.

Supplementary Text

Selection of calibration clades and fossils

Because the oldest fossil that belongs to a clade plays a critical role in setting the minimum

possible age for a clade, we first based the selection of calibration nodes on the existence of a

good quality and formally described fossil composed of multiple bones and whose affinities were

established by phylogenetic analysis or the presence of unambiguous derived characteristics. To

ensure all major avian groups contained at least one calibration node, in a few instances we

considered fossils consisting of a single bone if their phylogenetic position was unequivocal (see

below and data set 1 for details). Once a candidate clade was identified, we searched the

literature for the first fossil occurrence of each clade in each of nine major geographic regions of

the world: South America, North America, Europe, Africa, Madagascar, Asia, Australia

(including New Guinea), Zealandia, and Antarctica. For oceanic birds, we also ensured that

records in different continents were not in close proximity in the same oceanic region and

conversely, in some instances we included fossils from the same continent if they came from

different oceanic coasts. We started from global and regional compilations of fossil birds (29,

126–129), complemented by searches in the Paleobiology Database (http://fossilworks.org) and

Google Scholar (http://scholar.google.com). We evaluated each candidate fossil individually

based on the original descriptions and subsequent published analyses. In two instances, the

geographic origin of the clade was unquestionable (Casuariiformes, Artamidae); in those cases,

we used the oldest record of each fossil species (see data set 1) to generate the age prior.

The likelihood function used to generate a distribution for clade age assumes that fossil finds are

distributed uniformly through time (36, 37). We tested for departures from a uniform distribution

using a Kolmogorov-Smirnov test in R (function ks.test). The test requires that the minimum and

maximum bounds of the distribution are known, so we used point estimates of these bounds

using Ref. (38) equations 4 and 6. In cases of significant departure from uniformity, we

discarded the clade entirely or excluded late Paleogene and Neogene fossils. The final list of

calibration clades and fossils is given in data set 1. Cases in which the published evidence for the

phylogenetic position of the oldest fossil is controversial are discussed next.

Palaeognathae. We used two alternative calibrations for Palaeognathae. For the RAG dataset, we

used Diogenornis fragilis Alvarenga 1983, considered the oldest record of stem Rheiformes (29,

130), as the oldest fossil of a clade of "higher ratites" (all crown- paleognaths except for

Struthioniformes) (12, 131–133). Although Diogenornis has not been included in a phylogenetic

analysis, the fossil shows marked similarity to extant Rheidae. For the genome dataset, we used

an alternative calibration based on Lithornis. A recent analysis combining molecular and

osteological data placed Lithornis as sister to Tinamiformes and thus part of crown

Palaeognathae (133).

Crown Casuariiformes. The fossil genus Emuarius from the late Oligocene and early Miocene of

Australia sets a minimum possible age for crown Casuariiformes (Casuariidae and Dromaiidae).

Emuarius gidju (Patterson & Rich 1987) from Riversleigh sites is now known from multiple

bones, including the cranium, the oldest being ca. 24 Ma, and its phylogenetic position as a stem

member of the Dromaiidae was confirmed by phylogenetic analysis (134). The slightly older (ca.

25 Ma) Emuarius guljaruba Boles 2001 from Lake Palankarinna, known only from a

tarsometatarsus, is very similar to E. gidju and may turn out to be the same taxon (134),

therefore, we tentatively treated E. guljaruba as the oldest fossil representing crown

Casuariiformes. Given the exclusive Australopapuan distribution of all fossil and extant

members of this clade, we used the first fossil find of all species from the Australian continent

(data set 2).

Anatidae/Anseranatidae. Vegavis iaai Clarke et al. 2005 from the latest Cretaceous of Antarctica

(67 Ma) is the best evidence of a representative of a modern avian order in the Cretaceous (9).

Although the use of Vegavis for calibration as been questioned (18, 135), its affinities have been

established by phylogenetic analysis (9) and its old age is consistent with the long stem branch of

Anatidae in uncalibrated molecular trees (28). We also used Vegavis iaai to set a minimum age

for Galloanseres in the genome dataset because nodes within Anseriformes were not sampled in

that dataset.

Pelecanoidea. Two contemporaneous fossil birds from the early Oligocene (Rupelian) of Africa

and Europe provide a minimum age constraint for the Pelecanoidea, the clade formed by the

families Peleanidae, Scopidae, and Balaenicipitidae. One is Goliathia andrewsi Lambrecht,

1930, known from an ulna and a distal tarsometatarsus from quarry M of the Jebel Qatrani

Formation, Egypt, assigned to the Balaenicipitidae (136, 137) but without an explicit

phylogenetic character analysis. New estimates suggest an age between 29.5 and 30.2 Ma for

quarry M (138). The other fossil is a nearly complete skull and mandible from Luberon, France,

that is identical in all details to extant pelicans (139). Together, these two fossils set a minimum

possible age for the Pelecanoidea.

Pandionidae/Accipitridae. The early Oligocene specimen PW-2004/7-LS is an ungual phalanx

identified as an ancient osprey (140). Although it is a single bone without a scientific name,

ungual phalanxes of ospreys are very characteristic and show two derived characters not

observed in other birds of prey (29, 140). For this reason, even if fragmentary, we consider this

fossil to belong to the Pandionidae and it becomes the earliest unambiguous record of the crown

clade formed by Pandionidae and Accipitridae.

Tyranni/Passeri (eupasseres). The early Oligocene Wieslochia weissi Mayr & Manegold 2006

was described as a passerine most similar to suboscines but whose subordinal affinities could not

be determined (141). However, like all suboscines of the suborder Tyranni, the ulna of

Wieslochia has a well-developed tuberculum ligamenti collateralis ventralis (141). The

corroboration of a sister relationship between Passeriformes and Psittaciformes and the basal

position of Acanthisittidae indicate that this morphology is a derived state of the suborder

Tyranni; Psittaciformes, Zygodactylidae, Acanthisittidae, and the suborder Passeri do not have a

well developed tuberculum (except for representatives of Hirundinidae and Bombycillidae,

(142)). A well-developed processus procoracoideus also suggests Tyranni affinities (141). In

contrast, characters that suggest a more basal position of Wieslochia are ambiguous. For

example, although six ossified tendinal canals are a synapomorphy of the hypotarsus of

Eupasseres (143), the ossification of the hypotarsus is variable in Tyranni and open (only

partially ossified) tendinal canals are found in several members of the Furnarioidea (144).

Therefore, we conclude that Wieslochia belongs in the suborder Tyranni and therefore sets a

minimum age for crown Eupasseres, the clade formed by Tyranni and Passeri. In addition, there

is an articulated hand (SMF 504) from Luberon, France, of the same age that also shows a

derived character of the Tyranni in the distal carpometacarpus (145). Older remains previously

attributed to Passeriformes (146) are too fragmentary and may not even belong to this order

(135), and other fairly complete specimens from the early Oligocene of Europe cannot be

assigned to any of the three passerine suborders (147, 148).

Certhioidea. Certhiops rummeli Manegold 2008, described from a tarsometatarsus from the early

Miocene of Germany, shows derived characteristics of members of the superfamily Certhioidea

that climb tree trunks (149). Although there is strong support for the Certhioidea, including the

non-climbing Troglodytidae and Polioptilidae, relationships within it are not well resolved, and

the climbing families Certhiidae and Sittidae may not form a clade (150, 151). In any case, short

internodes among Certhioidea families (151, 152) constrain the possible branching of the fossil

lineage to a narrow time window. Therefore, we use Certhiops to set a minimum age for crown

Certhioidea.

Emberizoidea (nine-primaried oscines). Palaeostruthus hatcheri Shufeldt 1913 was described

based on a complete maxillary rostrum from the late Miocene of Kansas, USA. Although no

formal phylogenetic analysis has been conducted, details of this complex bone allow assignment

to the Passerellidae, and the rostrum is extremely similar to the extant Ammodramus savannarum

(153). However, given the polyphyly of Ammodramus (154), implying rapid homoplastic

evolution, we consider relationships of Palaeostruthus within the family unresolved. Therefore,

Palaeostruthus sets a minimum age for the clade formed by Passerellidae and its sister group.

Because relationships among families in the Emberizoidea are not well resolved (155) we used

Palaeostruthus and the fossil record of the Emberizoidea to calibrate this radiation, represented

by Emberiza and Thraupis in the RAG dataset.

Optimal partitioning scheme and substitution model

For the RAG dataset, we determined an optimal substitution model and partitioning scheme

simultaneously using the PartitionFinder algorithm (114). The maximally partitioned scheme

evaluated consisted of a partition by both gene and codon position (six partitions). A preliminary

maximum likelihood tree was generated using the maximally partitioned scheme and GTR +

Gamma models of substitution in RAxML (156) and used in PartitionFinder. The scheme that

minimized the Bayesian information criterion was nearly maximally partitioned with GTR +

Gamma models for most partitions except for the second codon position of RAG2 that was

grouped with the first codon position of RAG1, and the model for the third codon position of

RAG1 that had equal base proportions (the SYM + Gamma model, Ref. 157).

Bayesian divergence estimation and evaluation of priors

We ran the main analyses using a birth-death tree prior with incomplete sampling (158) that

takes into account that we sampled a small fraction of all avian species diversity; using the

‘birth-death skyline contemporary’ prior, part of the BEAST BDSKY 1.1.0 add-on (159), we set

a uniform prior (0, infinity) for the birth/total death ratio (effective reproduction number R0), a

uniform prior (0, infinity) for the “total death” rate (“become uninfectious”) prior, and a prior for

the sampling probability (rho) to take into account uncertainty regarding the total number of

extant avian species: we set the parameters of a beta distribution so that it resulted in a bell-

shaped distribution with the 5% quantile at 0.023, the proportion of the currently assumed 10,000

avian species in the RAG dataset (0.0048 for the genome dataset), and the 95% quantile at 0.008

(0.0016 for the genome dataset), corresponding to assuming about 30,000 extant avian species.

The sample from the prior showed that all clade-age priors behaved as expected except for the

prior on the Tyranni-Passeri (Eupasseres) clade, which produced much older ages than the

empirical density based on fossils. We suspect that this is an effect of the tree prior inducing an

old age for a clade of high diversity like Eupasseres. A more restrictive calibration density–

Gamma (1.3, 0.7)–was required to produce a prior similar to the empirical density.

We also repeated the analysis with a simple Yule prior to assess the sensitivity of our results to

tree prior specification. The tree prior had a noticeable influence on the results. With the Yule

tree prior, which assumes that all extant species are included, younger divergences are

underestimated and basal divergences overestimated when compared to the birth-death-sampling

prior (Fig. S5). This effect is expected given that deleting terminals from a phylogenetic tree

randomly results in relatively longer terminal branches and shorter basal branches. The genomic

dataset was more robust to the effect on younger divergences but not on basal divergences (Fig.

S5). On the other hand, age estimates around the K-Pg transition are not affected much by the

different tree priors. This effect of the tree prior may be a common cause of overestimation of

basal ages in divergence time estimation, increasing the gap between fossils and molecular

estimates, even when using genomic datasets. Therefore, careful selection and justification of the

tree prior and evaluation of its effects should be integral part of any Bayesian divergence time

study.

The final analysis used the birth-death-sampling prior. The first 12 million generations were

discarded for each of the six MCMC runs, after which all traces showed stationarity. All runs

converged and ESS values were above 200 for all parameter except for the age of Eupasseres,

which we attribute to the conflict between the tree prior and the calibration density mentioned

above. The coefficient of variation of the clock rate was between 0.63 and 0.80 (95% highest

posterior density), indicating that a lognormal relaxed clock was an appropriate model of rate

heterogeneity across lineages (i.e. the data were not strictly clock-like nor conforming to an

exponential relaxed clock).

Ancestral area reconstruction

Areas for ancestral reconstruction were a mixture of traditional classifications of zoogeographic

regions (160) and major continental landmasses, reflecting a compromise between current

patterns of distribution of clades and the history of paleogeographic configuration of the

continents. We did not use the Neotropical region as an area; its northern limits lie on the North

American and Caribbean plates but many of its component taxa are clearly of South American

origin (e.g. Tinamidae, New World suboscine passerines). Conversely, some Central American

and Caribbean taxa considered Neotropical may have originated in the tropical southern realms

of the North American continent (e.g. Todidae). For Africa, we considered the Afrotropical

region for coding taxa since taxa of northern arid lands (including the Arabic peninsula) have

clear Palearctic affinities. The Australian continent (including New Guinea) and Zealandia

(including New Caledonia) were treated as two different regions.

To explore the effects of different methodological assumptions and tree topologies, we

performed two additional biogeographic reconstructions. First, we used a dispersal-vicariance

likelihood model (DIVA-like) implemented in the library BioGeoBEARS in R (118). DIVA-like

is a probabilistic model implementation of the parsimony-based DIVA algorithm, (161), in

which dispersal, speciation, and extinction are modeled in an explicit way; in particular, DIVA

includes a classic vicariance scenario in which speciation results in the split of a widespread

ancestral geographic range. No dispersal matrices or time stratification were used. This analysis

was performed using the same tree as our main analysis. Second, we reconstructed ancestral

areas using Fitch parsimony (116) but using an alternative tree topology. We rearranged the

MCC tree of our RAG dataset so it matched the topology of a new proposed tree for Neornithes

(4). This new topology has several differences with our MCC, especially at the base of the

Neoaves radiation. After rearranging our MCC tree in Mesquite (162), we recovered an

ultrametric tree again by using the “mean path length” algorithm (163) implemented in the

function chronoMPL in the ape library (164). Finally, we added the fossil taxa as before and

reconstructed ancestral areas using function ancestral.pars in the phangorn library (119) with the

option MPR to obtain all possible parsimony reconstructions.

These two alternative methods resulted in ancestral area reconstructions similar to those of the

main analysis (compare Fig. S2 and Fig. S3). All analyses identified South America as the

ancestral area of Neornithes and its three main subclades Palaeognathae, Galloanseres, and

Neoaves. Therefore, this result is robust to changes in model assumptions and tree topology.

Because the DIVA-like model favors ancestors distributed across multiple areas before

speciation, a signal of dispersion out of South America appears earlier than in the Fitch

optimization in which area transitions can occur anytime along the descendant branches. The

alternative analyses show greater uncertainty regarding the ancestral area of Passeriformes and

Psittaciformes, for which the DIVA-like reconstruction includes Australia and Zealandia, in

addition to South America, as possible ancestral areas, suggesting earlier trans-Antarctic

connections and the alternative topology resulted in nearly complete ambiguity (Fig. S3). The

DIVA-like reconstruction favors Holarctic regions for stem nodes of Psittaciformes,

Cariamiformes, and the Steatornithidae-Nyctibiidae clade, which would imply an early

participation in the North American Gateway and then recolonization of Gondwanan continents.

Alternatively, this may be explained by the influence of the fossil taxa Halcyornithidae,

Idiornithidae, Prefica, and Paraprefica, distributed in the northern continents; the fact that they

are temporally closer to the ancestral node makes them more influential than extant taxa in

probabilistic ancestral-area estimation.

Reconstruction of Late Cretaceous-Cenozoic avifaunas

Traditionally, reconstructions of biotas at a point in space and time have been based largely on

direct fossil evidence, which is the gold standard for such inferences. The avian fossil record,

while steadily improving, is neither dense nor evenly distributed across the continents but instead

is better represented in the Northern Hemisphere (Mayr 2009). Our reconstructions of the

taxonomic composition of five global avifaunas (Table S2) are based on a synthesis of data from

phylogenetic relationships, the biogeographic and timetree reconstructions of stem-lineages (Fig.

1), and the Paleogene fossil record. We also incorporated knowledge of paleogeography to infer

movements of these avifaunas among continents. For example, we inferred presence in North

America for taxa of South American origin that reached the Old World (implied by the North

American Gateway Hypothesis). The goal is to infer where stem-lineages were distributed in

space and time across the avian tree. By integrating diverse lines of evidence it is therefore

possible to erect hypotheses about the inclusion of a taxon (stem-lineage) in an avifauna even

when there may currently be no direct fossil evidence for its presence (Table S2). This inference

instead comes from the other data just noted.

Taxonomic notes and biogeographic interpretations

Palaeognathae. Few problems in avian history have persisted over time than the

interrelationships and biogeography of the palaeognathous birds. Recent analyses using large-

scale data sets of both nuclear and mitochondrial DNA, some of which overlaps among studies,

have postulated that the flightless ratites are not monophyletic and that tinamous are imbedded

inside them, close to moas (12, 131, 132). These studies, and those based on whole

mitochondrial genomes (133, 165), have been unable to resolve several key nodes within

palaeognaths, although all place the root of the tree between ostriches and the other taxa. All

these studies make the assumption that losing flight multiple times is evolutionarily "easier" than

is regaining it (in the case of tinamous), therefore different studies postulate multiple long-

distance dispersal events across oceans to explain palaeognath distribution on the lands of

Gondwana. We think there is still much to learn about palaeognath history, and therefore remain

agnostic in this paper about the details of biogeographic scenarios. Our analysis strongly argues

for an origin of palaeognaths on Gondwana, and even most of the phylogenetic scenarios of

previous authors are largely consistent with vicariance among the southern continents of

flightless stem-lineages, even accepting several independent losses of flight. The most

perplexing finding is that of the proposed relationships of elephant-birds and kiwis (133), which

is based only on whole mitochondrial genomes. We await further evidence based on nuclear loci

before speculating on their biogeographic history.

Our parametric biogeographic (Fig. S3) and avifaunal reconstructions, as well as the fossil

record, suggest crown palaeognaths were broadly distributed in the Northern Hemisphere

certainly by the Paleocene and perhaps much earlier. Multiple fossil taxa are known from the

early Paleogene of North America and Europe (Mayr 2009), and the long stem-lineage of

palaeognaths suggests they may have been present there sometime in the Cretaceous. The most

viable hypothesis at this time is that one or more lineages were transferred from South to North

America in Cretaceous-Paleocene times and then to Eurasia, where lithornithids and various

Eurasian fossil groups evolved. We also propose that this stem-lineage may have included the

ostriches. The latter have been suggested as being related to Paleogene taxa in the Northern

Hemisphere (Mayr 2009), but that hypothesis needs further corroboration.

Kagu-Sunbittern-Aptornis. The relationship between the flightless New Caledonian Kagu

(Rhynochetus jubatus) and the Neotropical Sunbittern (Eurypyga helias) has been well supported

in multiple studies, and their relationship to other birds (tropicbirds, Phaethontidae) has

apparently been solved with whole-genome studies (3). Our analysis is consistent with a late

Paleogene vicariance event among South America, Australasia, and Zealandia, although at

present these taxa have no fossil record on Australia. We note that the flightless Miocene-Recent

New Zealand fossil Aptornis is suggested to be related to the Kagu (166, 167), although others

have questioned this relationship (168). Placement of Aptornis in the Kagu-Sunbittern clade

would further suggest a vicariance interpretation for this group.

Caprimulgiformes. Relationships among caprimulgiform higher-taxa are still poorly resolved

(169). Our time-tree and biogeographic analysis suggest that their diversification began in South

America during the Paleocene, with most lineages subsequently participating in the North

American Gateway or the trans-Antarctic route (Fig. S2). Contrary to recent suggestions of a

Palearctic origin and subsequent colonization of South America (169, 170), we found that stem-

hummingbirds are most likely South American in origin (Fig. S2, S3), although some early

lineages reached the Palearctic during the Eocene (171, 172).

Gruiformes, Charadriiformes, Opisthocomidae. Phylogenomic analysis recovered Opithocomus

as the sister-group of Charadriiformes and Gruiformes (3). This entire clade optimizes to South

America (West Gondwana) and its origins are estimated to be around the K-Pg transition. The

single species of extant Opisthocomidae, the Hoatzin (Opisthocomus hoatzin), is tropical

northern South American and fossils on that continent are recorded from the Miocene of

Colombia (173) and the late Oligocene-early Miocene of Brazil (174). Fossil Opisthocomiformes

have been found in the Old World, including the early Miocene of Namibia (174) and Kenya

(175) as well as the Eocene of France (176). Motivated by these findings, the argument has been

advanced that opisthocomids arose in the Old World and that the current South American

distribution is relictual (174, 176). This "out of Africa" hypothesis is taken in isolation without

information about higher-level relationships. Relationships among fossil and living taxa are also

poorly resolved (176) although the latter authors suggested that the Namibian taxon Namibiavis

is sister to all others. However, the relationships of opisthocomids to both Gruiformes and

Charadriiformes (3) as well as our global biogeographic reconstruction (Fig. 3, Fig. S2) indicate

that a South American, not an African, origin is most parsimonious. Probabilistic biogeographic

reconstructions are highly ambiguous, including South America, the Palearctic, and Africa, as

possible ancestral regions (Fig. S3). Until opisthocomids can be shown to be related to an Old

World taxon, the hypothesis that they were part of an early Paleogene North American biota that

moved into the tropical-subtropical western Palearctic via a North Atlantic land connection

explains more observations than fossil locality alone.

The Gruiformes are now restricted to the Ralloidea and Gruoidea (1, 28). Our optimization

recovers a South American (West Gondwana) origin, which follows from basal gruoids being

Neotropical (Psophiidae) and that the sister-group of the gruiforms is the Charadriiformes (3),

which are also South American in origin. Probabilistic models are more ambiguous, including

Africa as a possible ancestral area (Fig. S3). We recognize that gruiform biogeography is

complicated by an incomplete understanding of the phylogenetic placement of Paleogene fossils

relative to living gruoids as well as a very poor understanding of relationships among living and

fossil Ralloidea. Yet, given the evidence that gruiforms are related to charadriiforms, our

biogeographic hypothesis is the most robust to date.

Psittaciformes and Passeriformes. These two sister-taxa optimize as South American/West

Gondwanan in origin due to their basal relationships and the fact their immediate outgroups

(falconids and the Cariamae) themselves are South American in origin (Fig 2, Fig. S2). Setting

our limited sampling of parrots in the context of the larger sampling by previous authors (177–

179), our analysis is consistent with a West Gondwanan origin. On our time-tree, parrots show

two trans-Antarctic divergences involving South America, one for the Australian radiation and

the other for Zealandia. The distributions of outgroups suggest these were two temporally-

independent biotic interchanges from South America to East Gondwana, but future evidence may

indicate the New World radiation came from East Gondwana, as suggested by the probabilistic

reconstructions (Fig. S3). Participation in the North American Gateway is also evident, given the

presence of early lineages in the Paleogene of the Northern Hemisphere (29, 180).

A similar argument might be made for the early divergences of Passeriformes, with one event

involving the Acanthisitti of New Zealand and a second involving the Passeri. The results of this

paper confirm that the use of a geologically calibrated age of ~84-82 Ma for the biogeographic

split of Zealandia and West Antarctica for both passerines (23–25, 82) and parrots (177) was

inappropriate. Fossils that can be assigned to crown Passeriformes do not appear until the early

Oligocene around 32 Ma (135, 181). We found the age of Passeriformes difficult to estimate

because of the influence of the tree prior, as mentioned above, and some discrepancy between

datasets (genomic dataset: 46.1, 39.8-51.5 Ma; RAG dataset: 53.0, 48.5-58.0 Ma). In any case,

our new estimates place the most recent common ancestor of extant Passeriformes in the late

Paleocene or early Eocene. The gap between the estimated passerine crown-age and its first

crown fossils may be partially explained by the scarcity of avian fossiliferous beds in the

Paleogene of the southern continents, where passerines began their diversification (23, 24).

Supplementary diversification analyses

We evaluated whether the pattern of diversification through time was influenced by the

megadiverse order Passeriformes by pruning Passeriformes out of the tree and repeating the

estimates. The analysis without Passeriformes showed trends in net diversification rates similar

to those of the analysis with all Neornithes (Fig. S4D). Noticeable differences include higher

rates around the K-Pg boundary and during the late Oligocene-early Miocene warm period. The

latter effect resulted in a nearly monotonic increase in rates from the middle Eocene to the

present.

To evaluate the relative role of climate change, mass extinctions, and post-extinction bursts (big-

bangs) as drivers of diversification patterns, we used birth-death-shift models (120). Mass

extinction models included constant background speciation and extinction rates punctuated by

instantaneous mass extinctions (modeled as sampling events with function bd.ME.optim.rho) at

the K-Pg and Eocene-Oligocene transitions. The other two models included shifts in

diversification rates at specified times (function bd.ME.optim): in big-bang models, rates were

different 10 Ma after mass extinction events, and in ‘climate shifts’ models, rate shifts coincide

with major changes in global temperature. An overall sampling proportion of 0.0228 was used

since bd.ME.optim.rho cannot use information on richness for each terminal. No rate-shift was

modeled within the last 10 Ma since there were no branching events sampled in the time-tree.

We compared models using an information-theoretic approach based on the Akaike Information

Criterion and related metrics (182). The statistical comparison of alternative factors affecting

avian diversification dynamics using birth-death-shift models strongly favored a model in which

shifts in diversification rates coincided with major changes in global temperature (model

probability = 1, Table S4).

Supplemental Figures

Fig. S1. Probability density distributions for the age of the most recent common ancestor

(crown age) of 24 avian clades in the RAG data set inferred from the distribution of fossil

occurrences. Gray vertical lines indicate the age of the oldest fossil, including uncertainty. Red

lines show the empirical probability distribution of clade age obtained using the approach

outlined in Fig. 1. When the age uncertainty of the youngest or oldest fossil was greater than 1

Ma, the empirical distribution is the average of 500 pseudoreplicates based on ages uniformly

sampled from a time interval representing the uncertainty. Black lines are exponential or

lognormal probability density functions that mimic the empirical distributions and were

implemented as calibration priors in divergence time estimation (Table S1).

60708090 100110

Palaeognathae

6080100120140160 180

higher ratites

2530354045 5055

Casuariiformes

80100120 140

Galloanseres

80100120140 160

Anseranatidae/Anatidae

25303540 4550

Anserinae/Anatinae

20406080 100120

Odontophoridae/Phasianidae

304050 6070


25303540 4550

Columbidae

60708090 100

Caprimulgiformes

60708090 100

Cursorimorphae

607080 90100

Gruiformes

30405060 7080

Chionoidea

60708090 100110

Phaethontimorphae

6080100120 140

Procellariimorphae

50607080 90100

Suloidea

30405060 7080

Pelecanidae/Balaenicipitidae

40506070 8090

Pandionidae/Accipitridae

6080100 120140

Coraciimorphae

2530354045 5055

Picumninae/Picinae

1520253035 404550

Polyborinae/Falconinae

55606570 7580

Psittacopasserae

303540455055 6065

eupasseres

203040 50

Artamidae

20304050 6070

Certhioidea

10152025 30

Emberizoidea


Lik

elih

oo

d/P

rob

ab

ility

P.Pl.MioceneOligoceneEocenePaleoceneLateQNeogenePaleogeneCretaceous

90 80 70 60 50 40 30 20 10 0

Struthio camelus

Rhea americanaTinamus guttatusNothoprocta

Dromaius novaehollandiaeCasuarius casuarius

Apteryx australis

Megapodius freycinetLeipoa ocellataCrax blumenbachiiGuttera pucheraniCallipepla californicaRollulus rouloulGallus gallusBonasa umbellus

Chauna torquataAnseranas semipalmataDendrocygna arboreaAnser albifronsAnas platyrhynchos

Phoenicopterus ruberTachybaptus ruficollisPodiceps cristatusColumba liviaTreron calvaPterocles personatusMesitornis unicolor

Rhynochetus jubatusEurypyga helias

Phaethon lepturus

Otis tardaTauraco erythrolophus

Coccyzus americanusCentropus phasianinusCoua cristata

Guira guira

Aegotheles insignisHemiprocne mystaceaStreptoprocne zonarisChaetura pelagicaPhaethornis griseogularisFlorisuga mellivoraColibri coruscans

Nyctibius grandis

Steatornis caripensis

Podargus strigoidesBatrachostomus septimus

Eurostopodus macrotisCaprimulgus longirostris

Opisthocomus hoazin

Psophia crepitansGrus canadensis

Heliornis fulicaSarothrura insularis

Rallus limicola

Burhinus capensisChionis minorPluvianus aegyptius

Haematopus aterRecurvirostra americana

Charadrius vociferus

Thinocorus orbignyianusRostratula benghalensisJacana jacana

Scolopax rusticola

TurnixStiltia isabella

Catharacta skuaAlca torda

Larus marinus

Gavia immerAptenodytes forsteriSpheniscus humboldtiThalassarche bulleri

Pelecanoides magellaniOceanites oceanicus

Puffinus creatopus

Ciconia abdimiiTheristicus melanopis

Egretta tricolorPelecanus erythrorhynchusBalaeniceps rex

Anhinga anhingaPhalacrocorax

Fregata minorSula sula

Cathartes auraSagittarius serpentariusPandion haliaetusElanus caeruleusButeo jamaicensisNinox novaeseelandiaeStrix occidentalisTyto albaPhodilus badius

Leptosomus discolor

Colius colius

Trogon personatus

Tockus camurusBuceros bicornisPhoeniculus purpureusUpupa epops

Galbula albirostrisBucco capensis

Megalaima oortiLybius hirsutusTrachyphonus erythrocephalus

Capito nigerSemnornis frantzii

Pteroglossus aracari

Indicator variegatusMelanerpes carolinus

Merops pusillus

Todus angustirostris

Momotus momotaAlcedo leucogasterHalcyon malimbicaChloroceryle americana

Brachypteracias leptosomusCoracias caudata

Cariama cristata

Micrastur gilvicollisDaptrius aterFalco peregrinusNestor notabilisCalyptorhynchus funereus

Psittacus erithacusMyiopsitta monachus

Alisterus scapularis

Acanthisitta chlorisPitta sordida

Smithornis rufolateralisPsarisomus dalhousiaePhilepitta castanea

Sapayoa aenigma

Piprites chlorisPlatyrinchus coronatus

Rhynchocyclus brevirostris

Onychorhynchus coronatus

Oxyruncus cristatus

Tityra semifasciata

Cotinga cayana

Pipra coronataTyrannus tyrannus

Thamnophilus nigrocinereusTerenura sharpeiMelanopareia torquataConopophaga ardesiacaScytalopus magellanicusGrallaria ruficapilla

Sclerurus mexicanusFormicarius colma

Furnarius rufusMenura novaehollandiaeAtrichornis clamosusClimacteris erythropsPtilonorhynchus violaceus

Malurus melanocephalusMeliphaga analoga

Pardalotus punctatus

Petroica cucullata

Irena cyanogaster

Orthonyx teminckii

Nicator chloris

Mohoua albicilla

Pomatostomus isidorei

Lanius excubitor

Vireo philadelphia

Ptilorrhoa caerulescens

Struthidea cinerea

Daphoenositta chrysoptera

Pachycephala hyperthra

Cyanocitta cristata

Melampitta lugubris

Manucodia atraParadisaea raggiana

Cracticus quoyiArtamus leucorhynchus

Oriolus xanthonotus

Coracina novaehollandiae

Rhipidura hyperthraDicrurus adsimilis

Elminia nigromitratus

Monarcha axillaris

Aegithina tiphiaTelophorus dohertyiPrionops plumatus

Batis mixta

Vanga curvirostris

Philesturnus carunculatus

Chaetops frenatusPicathartes gymnocephalus

Bombycilla garrulus

Cinclus cinclusCatharus ustulatusMuscicapa ferruginea

Sturnus vulgarisMimus patagonicus

Sitta carolinensisCerthia familiarisTroglodytes aedon

Remiz pendulinusParus major

Aegithalos iouschensisHirundo rustica

Regulus calendula

Acrocephalus newtoni

Megalurus palustrisSphenoeacus afer

Pycnonotus barbatus

Cisticola anonymus

Zosterops senegalensis

Sylvia nana

Alauda arvensis

Promerops cafer

Dicaeum aeneum

Nectarinia olivacea

Melanocharis nigra

Paramythia montium

Prunella collarisPloceus cucullatus

Passer montanusMotacilla cinerea

Taeniopygia guttata

Fringilla montifringillaCalcarius lapponicusEmberiza schoeniclusThraupis cyanocephala

Struthio sp.

DinornithidaeLithornithidae

Aepyornithidae

Gallinuloididae

Presbyornithidae

Fluvioviridavidae

Prefica

Paraprefica

Eurotrochilus

ProtoazinNamibiavis

Rhynchaeitinae

SandcoleidaeChascacocolius

Plesiocathartes

Primotrogon

PrimobuccoEocoracias

Paracoracias

Palaeotodus

Messelirrisor

PhororhacoideaIdiornithidae

Halcyornithidae


Holocene

Zealandia

PalearcticNearctic

Australia

South America

Indomalay

Afrotropical

MadagascanPetroicidaeParoidea

Phaethontimorphae

Sphenisciformes

Dinornithiformes

Eurylaimides

AcanthisittidaePsittaciformes

Falconiformes

Tyrannides

Furnariides

MenuroideaMeliphagoidea

Passeroidea

Muscicapoidea

Certhioidea

Sylvioidea

Corvoidea

Orthonychidae

Bombycilloidea


Cariamiformes

BucerotiformesTrogoniformesLeptosomiformesColiiformesStrigiformes

Accipitriformes

Procellariiformes

Gaviiformes

Charadriiformes

Coraciiformes

Piciformes

Gruiformes

Opisthocomiformes

Caprimulgiformes

Cuculiformes Otidiformes

MusophagiformesColumbimorphae

Galliformes

Anseriformes

Casuariiformes

Struthioniformes

Apterygiformes

Tinamiformes

Rheiformes

Pelecaniformes

Passeriform

es

TyranniP

asseridesC

orvides

Coraciornithia

Aequornithia

Fig S2. Biogeographic ancestral area reconstruction using Fitch parsimony optimization. Ancestral area reconstructions using the Fitch algorithm are shown on the Maximum Clade

Credibility tree from the Bayesian divergence time estimation of 230 species of Neornithes with

the addition a posteriori of 25 fossil taxa that represent Holarctic distributions for clades

currently restricted to the tropics. All possible most parsimonious reconstructions are shown for

each node. Distributions at the tips are those of the clades they represent.

PPMioceneOligoceneEocenePaleoceneLateNeogenePaleogeneCretaceous

90 80 70 60 50 40 30 20 10 0

Struthio camelusStruthio sp.

Rhea americanaTinamus guttatusNothoprocta

LithornithidaeDinornithidaeApteryx australisAepyornithidaeDromaius novaehollandiaeCasuarius casuariusChauna torquataAnseranas semipalmataDendrocygna arboreaAnser albifronsAnas platyrhynchos

PresbyornithidaeMegapodius freycinetLeipoa ocellataCrax blumenbachiiGuttera pucheraniCallipepla californicaRollulus rouloulGallus gallusBonasa umbellus

GallinuloididaePhoenicopterus ruberTachybaptus ruficollisPodiceps cristatusColumba liviaTreron calvaPterocles personatusMesitornis unicolorTauraco erythrolophusOtis tardaGuira guiraCoccyzus americanusCentropus phasianinusCoua cristataPodargus strigoidesBatrachostomus septimus

FluvioviridavidaeEurostopodus macrotisCaprimulgus longirostrisNyctibius grandis

ParapreficaSteatornis caripensis

PreficaAegotheles insignisHemiprocne mystaceaStreptoprocne zonarisChaetura pelagicaPhaethornis griseogularisFlorisuga mellivoraColibri coruscans

EurotrochilusOpisthocomus hoazin

ProtoazinNamibiavis

Psophia crepitansGrus canadensisRallus limicolaHeliornis fulicaSarothrura insularisBurhinus capensisChionis minorPluvianus aegyptiusCharadrius vociferusHaematopus aterRecurvirostra americanaScolopax rusticolaThinocorus orbignyianusRostratula benghalensisJacana jacanaTurnixStiltia isabellaLarus marinusCatharacta skuaAlca tordaPhaethon lepturusRhynochetus jubatusEurypyga heliasGavia immerAptenodytes forsteriSpheniscus humboldtiThalassarche bulleriOceanites oceanicusPelecanoides magellaniPuffinus creatopusFregata minorSula sulaAnhinga anhingaPhalacrocoraxCiconia abdimiiTheristicus melanopis

RhynchaeitinaeEgretta tricolorPelecanus erythrorhynchusBalaeniceps rexCathartes auraSagittarius serpentariusPandion haliaetusElanus caeruleusButeo jamaicensisNinox novaeseelandiaeStrix occidentalisTyto albaPhodilus badiusColius colius

ChascacocoliusSandcoleidae

Leptosomus discolorPlesiocathartes

Trogon personatusPrimotrogon

Tockus camurusBuceros bicornisPhoeniculus purpureusUpupa epops

MesselirrisorMerops pusillusBrachypteracias leptosomusCoracias caudata

ParacoraciasEocoracias

PrimobuccoTodus angustirostris

PalaeotodusMomotus momotaAlcedo leucogasterHalcyon malimbicaChloroceryle americanaGalbula albirostrisBucco capensisIndicator variegatusMelanerpes carolinusMegalaima oortiLybius hirsutusTrachyphonus erythrocephalusSemnornis frantziiCapito nigerPteroglossus aracariCariama cristata

IdiornithidaePhororhacoidea

Micrastur gilvicollisDaptrius aterFalco peregrinusNestor notabilisCalyptorhynchus funereusMyiopsitta monachusPsittacus erithacusAlisterus scapularis

HalcyornithidaeAcanthisitta chlorisPitta sordidaSapayoa aenigmaSmithornis rufolateralisPsarisomus dalhousiaePhilepitta castaneaTyrannus tyrannusPipra coronataTityra semifasciataOnychorhynchus coronatusCotinga cayanaRhynchocyclus brevirostrisOxyruncus cristatusPiprites chlorisPlatyrinchus coronatusThamnophilus nigrocinereusTerenura sharpeiMelanopareia torquataConopophaga ardesiacaScytalopus magellanicusGrallaria ruficapillaFormicarius colmaSclerurus mexicanusFurnarius rufusMenura novaehollandiaeAtrichornis clamosusClimacteris erythropsPtilonorhynchus violaceusMeliphaga analogaMalurus melanocephalusPardalotus punctatusOrthonyx teminckiiPomatostomus isidoreiChaetops frenatusPicathartes gymnocephalusPhilesturnus carunculatusMohoua albicillaMelanocharis nigraVireo philadelphiaDaphoenositta chrysopteraCoracina novaehollandiaeParamythia montiumPtilorrhoa caerulescensPachycephala hyperthraOriolus xanthonotusBatis mixtaAegithina tiphiaTelophorus dohertyiPrionops plumatusVanga curvirostrisCracticus quoyiArtamus leucorhynchusRhipidura hyperthraDicrurus adsimilisLanius excubitorCyanocitta cristataManucodia atraParadisaea raggianaStruthidea cinereaMelampitta lugubrisMonarcha axillarisPetroica cucullataPromerops caferElminia nigromitratusRemiz pendulinusParus majorNicator chlorisAlauda arvensisSphenoeacus aferMegalurus palustrisCisticola anonymusAegithalos iouschensisHirundo rusticaAcrocephalus newtoniZosterops senegalensisPycnonotus barbatusSylvia nanaSitta carolinensisCerthia familiarisTroglodytes aedonSturnus vulgarisMimus patagonicusCinclus cinclusCatharus ustulatusMuscicapa ferrugineaNectarinia olivaceaIrena cyanogasterBombycilla garrulusRegulus calendulaDicaeum aeneumPrunella collarisPloceus cucullatusTaeniopygia guttataPasser montanusMotacilla cinereaFringilla montifringillaCalcarius lapponicusEmberiza schoeniclusThraupis cyanocephala


ocene

Zealandia

PalearcticNearctic

Australia

South America

Indomalay

Afrotropical

Madagascan

PPMioceneOligoceneEocenePaleoceneLateNeogenePaleogeneCretaceous

90 80 70 60 50 40 30 20 10 0

Struthio camelus

Rhea americanaApteryx australis

Tinamus guttatusNothoproctaDromaius novaehollandiaeCasuarius casuariusChauna torquataAnseranas semipalmata

Dendrocygna arboreaAnser albifronsAnas platyrhynchos

Megapodius freycinetLeipoa ocellataCrax blumenbachiiGuttera pucheraniCallipepla californicaRollulus rouloulGallus gallusBonasa umbellusEurostopodus macrotisCaprimulgus longirostrisNyctibius grandis

Steatornis caripensis

Podargus strigoidesBatrachostomus septimusAegotheles insignisHemiprocne mystaceaStreptoprocne zonarisChaetura pelagica

Phaethornis griseogularisFlorisuga mellivoraColibri coruscansColumba liviaTreron calvaPterocles personatusMesitornis unicolorTauraco erythrolophusOtis tardaGuira guiraCoccyzus americanusCentropus phasianinusCoua cristataPsophia crepitansGrus canadensisRallus limicolaHeliornis fulicaSarothrura insularisPhoenicopterus ruberTachybaptus ruficollisPodiceps cristatusBurhinus capensisChionis minorPluvianus aegyptiusCharadrius vociferusHaematopus aterRecurvirostra americanaScolopax rusticolaThinocorus orbignyianusRostratula benghalensisJacana jacanaTurnixStiltia isabellaLarus marinusCatharacta skuaAlca tordaPhaethon lepturusRhynochetus jubatusEurypyga heliasGavia immerAptenodytes forsteriSpheniscus humboldtiThalassarche bulleriOceanites oceanicusPelecanoides magellaniPuffinus creatopusCiconia abdimiiTheristicus melanopis

Egretta tricolorPelecanus erythrorhynchusBalaeniceps rexFregata minorSula sulaAnhinga anhingaPhalacrocorax

Opisthocomus hoazin

Cathartes auraSagittarius serpentariusPandion haliaetusElanus caeruleusButeo jamaicensisNinox novaeseelandiaeStrix occidentalisTyto albaPhodilus badiusColius colius

Leptosomus discolor

Trogon personatus

Tockus camurusBuceros bicornis

Phoeniculus purpureusUpupa epopsMerops pusillus

Brachypteracias leptosomusCoracias caudataTodus angustirostris

Momotus momotaAlcedo leucogasterHalcyon malimbicaChloroceryle americanaGalbula albirostrisBucco capensisIndicator variegatusMelanerpes carolinusMegalaima oortiLybius hirsutusTrachyphonus erythrocephalusSemnornis frantziiCapito nigerPteroglossus aracariCariama cristata

Micrastur gilvicollisDaptrius aterFalco peregrinus

Nestor notabilisCalyptorhynchus funereusAlisterus scapularisPsittacus erithacusMyiopsitta monachusAcanthisitta chlorisPsarisomus dalhousiaePhilepitta castaneaSapayoa aenigmaPitta sordidaSmithornis rufolateralisPipra coronataCotinga cayanaOnychorhynchus coronatusPlatyrinchus coronatusOxyruncus cristatusTityra semifasciataPiprites chlorisRhynchocyclus brevirostrisTyrannus tyrannusThamnophilus nigrocinereusTerenura sharpeiMelanopareia torquataConopophaga ardesiacaScytalopus magellanicusGrallaria ruficapillaFormicarius colmaSclerurus mexicanusFurnarius rufusMenura novaehollandiaeAtrichornis clamosusClimacteris erythropsPtilonorhynchus violaceusMeliphaga analogaMalurus melanocephalusPardalotus punctatusOrthonyx teminckiiPomatostomus isidoreiChaetops frenatusPicathartes gymnocephalusPhilesturnus carunculatusMohoua albicillaMelanocharis nigraVireo philadelphiaDaphoenositta chrysopteraCoracina novaehollandiaeParamythia montiumPtilorrhoa caerulescensPachycephala hyperthraOriolus xanthonotusBatis mixtaAegithina tiphiaTelophorus dohertyiPrionops plumatusVanga curvirostrisCracticus quoyiArtamus leucorhynchusRhipidura hyperthraDicrurus adsimilisLanius excubitorCyanocitta cristataManucodia atraParadisaea raggianaStruthidea cinereaMelampitta lugubrisMonarcha axillarisPetroica cucullataPromerops caferElminia nigromitratusRemiz pendulinusParus majorNicator chlorisAlauda arvensisSphenoeacus aferMegalurus palustrisCisticola anonymusAegithalos iouschensisHirundo rusticaAcrocephalus newtoniZosterops senegalensisPycnonotus barbatusSylvia nanaSitta carolinensisCerthia familiarisTroglodytes aedonSturnus vulgarisMimus patagonicusCinclus cinclusCatharus ustulatusMuscicapa ferrugineaNectarinia olivaceaIrena cyanogasterBombycilla garrulusRegulus calendulaDicaeum aeneumPrunella collarisPloceus cucullatusTaeniopygia guttataPasser montanusMotacilla cinereaFringilla montifringillaCalcarius lapponicusEmberiza schoeniclusThraupis cyanocephala

Struthio sp.

DinornithidaeLithornithidae

Aepyornithidae

Gallinuloididae

Presbyornithidae

FluvioviridavidaePrefica

Paraprefica

Eurotrochilus

Protoazin

Namibiavis

Rhynchaeitinae

SandcoleidaeChascacocolius

Plesiocathartes

Primotrogon

PrimobuccoEocoracias

Paracoracias

Palaeotodus

Messelirrisor

PhororhacoideaIdiornithidae

Halcyornithidae


A B

Fig S3. Alternative biogeographic ancestral area reconstructions. (A) Ancestral area

reconstructions using a dispersal-vicariance likelihood model. Pie charts on nodes show the

marginal probability of each geographic region. The tree is the Maximum Clade Credibility

(MCC) tree from the Bayesian divergence time analysis of the RAG dataset with the addition a

posteriori of 25 fossil taxa that represent Holarctic distributions for clades currently restricted to

the tropics. (B) Ancestral area reconstructions using Fitch parsimony on an alternative tree

topology (4) (see Supplementary Text for details).

A0

50100

Cra

ter

diam

eter

(km

)

ChicxulubChesapeake Bay

PopigaiB

2

4

6

Bas

alt

volu

me

(Mkm

3 )

Sierra Leone

Maud Rise Deccan North AtlanticEthiopian-Yemen

Columbia River

-2

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4

6

8

10

12

Dee

p oc

ean

tem

pera

ture

(°C

)

C

Late KCooling

P�-EoWarming

Early EoOptimum

Long-termEo Cooling

OG-1Glaciation

Late OGWarming

Mid-MlOptimum

Mid-MlCooling

PS

Glaciat.

D

0.02

0.05

0.10

0.20

0.50

Net

div

ersi

ficat

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rate

(Ma�

1 )

MioceneOligoceneEocenePaleoceneLate PSPO

QNeogenePaleogeneCretaceous

90 80 70 60 50 40 30 20 10 0


Fig S4. Diversification through time of modern birds and Earth history events. (A)

Meteorite impact crater data from (183) including only those larger than 10 km in diameter and

standard deviations of age estimates lower than 5 Ma. (B) Large igneous provinces: time range

of major activity and original volume from (184), to which we added the Sierra Leone and Maud

Rise Provinces from (185). (C) Deep-ocean paleotemperatures estimated from a global

compilation of benthic foraminifera oxygen isotope data (124) and equations 3.5 and 3.6 in

(125), represented by a local regression smoother and associated 95% confidence intervals.

Vertical dashed lines indicate the subdivision of time intervals with different climates used for

the “environmental shifts model” model. (D) Net lineage diversification rate (speciation -

extinction) estimated for 5 Ma intervals for all Neornithes (red line), excluding the order

Passeriformes (gray line and interquartile ranges), and the ‘environmental birth-death-shift

model’, in which intervals represent periods with different climates; lines are medians of 500

estimates from a sample of the posterior distribution of trees.

Fig. S5. Effect of the tree prior on Bayesian divergence time estimation. Maximum clade

credibility (MCC) trees from a Bayesian divergence time estimation assuming a “birth-death-

sampling” prior that incorporates the fact that the only a fraction of extant avian diversity was

included: (A) time-tree obtained using ~124 kilobases from the first and second codon position

of 1156 clock-like genes of 48 species (genomic dataset); (B) time-tree obtained using ~4

kilobases of the recombination-activating genes (RAG) of 230 species. Red arrows indicate the

displacement of nodes in relation to the MCC tree obtained using a simple Yule prior that

assumes complete species sampling (tree comparison used function compare.phylo in the

phyloch library in R, available at http://www.christophheibl.de/Rpackages.html).

11010090 807060 504030 20100


A B

1201008060 40200


Table S1. Probability distributions of clade age from fossil occurrences used as calibration priors in Bayesian

divergence time analysis in BEAST.

Crown clade Oldest fossil dataset n distribution μ σ offset

Palaeognathae Lithornis celetius genomic 8 log-normal 2.1 0.9 61.7

higher ratites Diogenornis fragilis RAG 4 log-normal 2.8 1.3 55.8

Casuariiformes Emuarius guljaruba RAG 6 log-normal 1.4 1.0 24.0

Galloanseres* Vegavis iaai genomic 7 log-normal 1.9 1.1 66.0

Anseranatidae/Anatidae* Vegavis iaai RAG 5 log-normal 1.5 1.0 66.0

Anserinae/Anatinae Mionetta blanchardi RAG 8 log-normal 1.5 0.8 23.0

Odontophoridae/Phasianidae Palaeortyx gallica RAG 4 log-normal 2.5 0.7 23.0

Phoenicopterimorphae Adelalopus hoogbutseliensis both 7 log-normal 1.6 0.7 30.0

Columbidae Primophaps schoddei RAG 7 log-normal 1.2 1.0 24.0

Caprimulgiformes Eocypselus vincenti both 7 exponential 9.0

54.0

Cursorimorphae Scandiavis mikkelseni both 7 exponential 9.0

54.0

Gruiformes Messelornis nearctica RAG 7 exponential 8.5

52.0

Chionoidea Wilaru tedfordi RAG 4 log-normal 1.9 1.1 24.0

Phaethontimorphae Lithoptila abounensis both 3 log-normal 1.4 0.7 55.8

Procellarimorphae Waimanu manneringi both 5 exponential 11.0

61.0

Suloidea Limnofregata azygosternon RAG 7 exponential 7.0

52.0

Pelecanidae/Balaenicipitidae Goliathia andrewsi RAG 5 log-normal 1.8 0.8 30.0

Pandionidae/Accipitridae PW-2004/7-LS RAG 6 log-normal 1.7 0.8 33.9

Coraciimorphae Sandcoleus copiosus both 5 exponential 14.0

56.4

Picumninae/Picinae Piculoides saulcetensis RAG 5 exponential 5.5

22.5

Polyborinae/Falconinae Pediohierax ramenta RAG 5 log-normal 1.7 0.8 16.0

Psittacopasserae* Pulchrapollia gracilis both 3 log-normal 1.0 1.5 55.4

eupasseres Wieslochia weissi both 7 log-normal 1.7 0.8 30.0

Artamidae Kurrartapu johnnguyeni RAG 2 log-normal 2.0 0.7 16.0

Certhioidea Certhiops rummeli RAG 3 log-normal 2.0 1.2 18.0

Emberizoidea Palaeostruthus hatcheri RAG 4 log-normal 1.0 1.0 9.0

Probability distributions are inferred using the method described in Fig. 1. n is the number of fossil occurrence used, μ and σ are the

parameters of the probability distributions. The offset for the prior distribution is the upper stratigraphic bound (minimum age) of its oldest fossil. For clades marked with *, late Paleogene and Neogene fossils were excluded to improve uniformity of fossil occurrences. See data set 1 for

details of the fossils used.

Table S2. Reconstructions of the taxonomic composition of Late Cretaceous–Cenozoic global avifaunas.

Late Cretaceous-early Paleogene West Gondwanan Avifauna

Confirmed by fossil record: Rheiformes, Galloanserae (including extinct Pelargornithidae),

Phoenicopterimorphae, Cariamiformes, Sphenisciformes, Gaviiformes, Charadriiformes, and Falconidae

Inferred from ancestral-area reconstructions and/or paleobiogeographic connectivity: Palaeognathae,

Rheiformes, Tinamiformes, Galloanseres, Anhimidae, Cracidae, Neoaves, Opisthocomiformes,

Phoenicopterimorphae (Phoenicopteridae + Podicipedidae), Caprimuligiformes, Steatornithidae,

Nyctibiidae, Apodi, Gruiformes, Charadriiformes, Phaethontimorphae, Eurypygiformes, Aequornithia,

Sphenisciformes, Gaviiformes, Coraciornithia, Cariamiformes, Falconiformes, Psittaciformes, and

Passeriformes.

Paleogene East Gondwanan avifauna

Confirmed by fossil record: Galloanserae, Anseriformes, Coracionithia?, Sphenisciformes,

Charadriiformes?, Passeriformes.

Inferred from ancestral-area reconstructions and/or paleobiogeographic connectivity: Dinornithiformes, Casuariformes, Apterygiformes, Galloanserae, Anseranatidae, Megapodiidae,

Podargidae, Charadriiformes, Rhynochetidae, Spenisciformes, Hemiprocnidae, Aegothelidae, Strigopidae,

Cacatuidae, Acanthisitti, Passeri.

Early to middle Paleogene Holarctic avifauna

Confirmed by fossil record: Palaeognathae, Struthioniformes, Lithornithidae, Galliformes, Phasianoidea,

Anseriformes, Mesitornithidae, Phoenicopteriformes, Otidimorphae including Cuculidae + Musophagidae

+ Otididae, Caprimulgiformes, Steatornithidae, Podargidae, Caprimulgidae, Nyctibiidae, Apodi,

Phaethontiformes, Opisthocomiformes, Grui (Messelornithidae?), Charadriiformes, Gaviidae,

Pelecaniformes, Coracornithia, Coraciimorphae, Leptosomidae, Coliidae, Trogonidae, Coraciidae,

Galbullae, Accipitriformes, Strigiformes, Cariamiformes, Psittacidae, Eurylaimides.


Struthioniformes, Lithornithidae, Galliformes, Cracidae, Phasianoidea, Anseriformes, Mesitornithidae,

Phoenicopteriformes, Otidimorphae including Cuculidae + Musophagidae + Otididae, Podargidae,

Caprimulgidae, Nyctibiidae, Apodi, Phaethontiformes, Opisthocomiformes, Grui (Messelornithidae?),

Charadriiformes, Gaviidae, Pelecaniformes, Coracornithia, Coraciimorphae, Leptosomidae, Coliidae,

Trogonidae, Coraciidae, Galbulae, Strigiformes, Accipitriformes, Strigiformes, Cariamiformes, Psittacidae,

Eurylaimides.

Paleogene African avifauna:

Confirmed by fossil record: Galloanserae (Pelargornithidae), Opisthocomidae, Phaethontiformes.


Galloanserae (including extinct Pelargornithidae), Opithocomidae, Columbimorphae, Otidimorphae,

Coracornithia, Buceroti + Coraciiformes, Balaenicipitidae.

Paleogene Malagasy avifauna:

Confirmed by fossil record: None

Inferred from ancestral-area reconstructions and/or paleobiogeographic connectivity: Leptosomiformes, Mesitornithiformes, Couinae, Brachypteraciidae, Philepittidae, and Vangidae.

Avifaunas reconstructed from stem-lineages of extant clades based on the Neornithes time-tree and ancestral-area reconstruction

(Fig. 3, fig. S2), paleogeographic models, and the avian fossil record. Paleobiogeographic connectivity was used for some clades

lacking fossils in an area and without ancestral reconstructions in the region but their presence is implied by the biogeographic

hypothesis (e.g., suboscines in the Paleogene of North America).

Table S3. Environmental birth-death models of the associations between diversification rates and global

temperature in modern birds

Environment-dependent function

Speciation Extinction K L-Lik AIC ΔAIC P

linear linear 4 -927.3 1862.6 0.0 1.00

linear constant 3 -939.6 1885.1 22.5 0.00

exponential constant 3 -940.1 1886.2 23.6 0.00

exponential exponential 4 -940.1 1888.2 25.6 0.00

constant exponential 3 -943.2 1892.5 29.9 0.00

constant linear 3 -943.2 1892.5 29.9 0.00

constant constant 2 -943.2 1890.4 27.8 0.00

Number of parameters (K), log-likelihood (L-Lik), Akaike information criterion (AIC), AIC difference (∆AIC),

and model probability (P).

Table S4. Birth-death shift models representing associations between Earth history events and

diversification rates in modern birds

Description K L-Lik AIC ΔAIC P

Shifts with temperature changes 14 -909.6 1847.2 0.0 1.00

Different rates during 10 Ma after E-OG 6 -931.5 1875.0 27.8 0.00

Different rates during 10 Ma after K-Pg and E-OG 10 -927.9 1875.8 28.6 0.00

E-OG mass extinction 3 -941.5 1889.0 41.8 0.00

Uniform birth-death model 2 -943.2 1890.4 43.2 0.00

K-Pg and E-OG mass extinctions 4 -941.6 1891.2 44.0 0.00

K-Pg mass extinction 3 -943.2 1892.5 45.3 0.00

Different rate during 10 Ma after K-Pg 6 -942.7 1897.4 50.1 0.00 Number of parameters (K), log-likelihood (L-Lik), Akaike information criterion (AIC), AIC difference (∆AIC),

and model probability (P).

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