rsos.royalsocietypublishing.org Australo ...rsos.royalsocietypublishing.org/content/royopensci/2/2/140375.full.pdf · chloris species complex (Aves: Alcedinidae) and its close relatives

rsosroyalsocietypublishingorg

ResearchCite this article Andersen MJ Shult HTCibois A Thibault J-C Filardi CE Moyle RG2015 Rapid diversification and secondarysympatry in Australo-Pacific kingfishers (AvesAlcedinidae Todiramphus) R Soc open sci2 140375httpdxdoiorg101098rsos140375

Received 14 October 2014Accepted 6 January 2015

Subject CategoryBiology (whole organism)

Subject Areastaxonomy and systematicsevolution

Keywordsisland biogeography diversification ratesdivergence time estimation great speciatorsTodiramphus chloris

Author for correspondenceMichael J Andersene-mail mandersenamnhorg

daggerPresent address American Museum ofNatural History Department of OrnithologyCentral Park West at 79th Street New York NY10024 USA

DaggerPresent address Department of EntomologyLife Sciences Building Louisiana StateUniversity Baton Rouge LA 70803 USA

Electronic supplementary material is availableat httpdxdoiorg101098rsos140375 or viahttprsosroyalsocietypublishingorg

Rapid diversification andsecondary sympatry inAustralo-Pacific kingfishers(Aves AlcedinidaeTodiramphus)Michael J Andersen1dagger Hannah T Shult1Dagger Alice

Cibois2 Jean-Claude Thibault3 Christopher E Filardi4dagger

and Robert G Moyle1

1Department of Ecology and Evolutionary Biology and Biodiversity Institute Universityof Kansas Lawrence KS 66045 USA2Natural History Museum of Geneva Department of Mammalogy and OrnithologyCP 6434 CH-1211 Geneva 6 6434 Switzerland3Museacuteum National drsquoHistoire Naturelle Deacutepartement Systeacutematique et EvolutionUMR7205 Case Postale 51 55 Rue Buffon 75005 Paris France4American Museum of Natural History Center for Biodiversity and ConservationCentral Park West at 79th Street New York NY 10024 USA

1 SummaryTodiramphus chloris is the most widely distributed of the Pacificrsquoslsquogreat speciatorsrsquo Its 50 subspecies constitute a species complexthat is distributed over 16 000 km from the Red Sea to PolynesiaWe present to our knowledge the first comprehensive molecularphylogeny of this enigmatic radiation of kingfishers Ten PacificTodiramphus species are embedded within the T chloris complexrendering it paraphyletic Among these is a radiation of fivespecies from the remote islands of Eastern Polynesian as well asthe widespread migratory taxon Todiramphus sanctus Our resultsoffer strong support that Pacific Todiramphus including T chlorisunderwent an extensive range expansion and diversificationless than 1 Ma Multiple instances of secondary sympatry haveaccumulated in this group despite its recent origin including onAustralia and oceanic islands in Palau Vanuatu and the SolomonIslands Significant ecomorphological and behavioural differencesexist between secondarily sympatric lineages which suggest thatpre-mating isolating mechanisms were achieved rapidly duringdiversification We found evidence for complex biogeographicpatterns including a novel phylogeographic break in the easternSolomon Islands that separates a Northern Melanesian clade

2015 The Authors Published by the Royal Society under the terms of the Creative CommonsAttribution License httpcreativecommonsorglicensesby40 which permits unrestricteduse provided the original author and source are credited

on September 27 2018httprsosroyalsocietypublishingorgDownloaded from

rsosroyalsocietypublishingorgRSocopensci2140375

from Polynesian taxa In light of our results we discuss systematic relationships of Todiramphus andpropose an updated taxonomy This paper contributes to our understanding of avian diversification andassembly on islands and to the systematics of a classically polytypic species complex

2 IntroductionClassic hypotheses about diversification of insular organisms are based on a relatively simple dynamicbetween colonization and extinction of allopatrically derived species [1ndash6] These ideas are beingchallenged however by phylogenies that support complex diversification and colonization scenarios(eg [7ndash9]) This re-evaluation of insular diversification has revealed extensive insular radiations withhigh sympatric diversity and subsequent re-colonization of continental areas Thus community diversityon islands depends not only on the flow of colonists from continental areas but also on the frequencyof secondary sympatry within insular lineages Furthermore a broad spectrum of lineage ages existsin island systems For example recent phylogenetic study has uncovered the ubiquity of insular avianlineages exhibiting recent allopatric diversification over large areas of the Pacific [10ndash12] providing acontext for high potential speciation rates Conversely lsquomaturersquo insular radiations exist with extensive co-occurrence of constituent taxa and substantial ecomorphological differentiation which often confoundedtraditional taxonomy [712ndash15]

The rate of attaining reproductive isolation and the build-up of sympatry (ie assembly) on islands isunderstudied in non-adaptive radiations (eg away from Hawaii and the Galaacutepagos [16ndash18]) A keycomponent is the critical stage after initial geographical expansion and subsequent diversification(ie allopatric speciation) when diversifying lineages initiate secondary sympatry among recentlydiverged populations Unfortunately most avian radiations are not suitable for studying the processof secondary sympatry on islands For example mature insular radiations provide only an incompletepicture because extinction changes in distribution and substantial anagenesis obscures early stagesof lineage accumulation whereas purely geographical radiations (eg [10]) have not yet begunthe process thus they are uninformative in the study of insular species assembly and secondarysympatry Evidence from mature continental radiations supports a scenario of substantial divergencein allopatry before lineages are able or have the opportunity to co-occur [1920] however factorsthat influence rates to secondary sympatry in continental systems are numerous complex geographyclosed ecological communities disease transmission biotic and abiotic environmental interactionsecological similarity of sister taxa and complex signalling environments [20ndash25] Conversely insularsystems are comparatively simple and may provide the most accessible insight into the tempo andmode of attaining secondary sympatry even though extrapolation to diverse continental systems isdifficult [17]

Here we examine the phylogeographic and temporal patterns of diversification in the Todiramphuschloris species complex (Aves Alcedinidae) and its close relatives This species complex is the mostwidespread of the archetypal lsquogreat speciatorsrsquo [26] and comprises 50 nominal subspecies spanninga distance more than 16 000 km from the Red Sea to Samoa [27ndash29] The full geographical extent ofthe genus extends a further 3000 km east to the Marquesas Islands in Eastern Polynesia (kingfishersdo not occur in Hawaii) Most nominal subspecies correspond to single-island populations that arephenotypically distinct in plumage and size but some islandsarchipelagos have multiple sympatricTodiramphus species including Palau Vanuatu and several islands in the Solomon Islands andthe Bismarck Archipelago as well as Australia These instances of sympatry are presumed to besecondary (ie after allopatric speciation) Additionally the distribution of Todiramphus sanctusmdashtheonly migratory Todiramphusmdashbroadly overlaps many congeners in the T chloris complex All sympatricTodiramphus exhibit ecological morphological and behavioural differences including separation byhabitat preference suggesting a high degree of reproductive isolation between each pair [272830]Previous phylogenetic work on higher level kingfisher relationships showed extremely low geneticdifferentiation among five Todiramphus species [31] but only one T chloris sample was included Withregard to non-adaptive (eg geographical) insular radiations the T chloris complex has several notablefeatures The broad distribution numerous instances of closely related sympatric species and closerelationship between migratory and sedentary species make the T chloris complex an ideal lineage forexamining the consequence of rapid diversification and subsequent assembly of secondarily sympatricspecies in an insular system

3 Material and methods31 Taxon samplingOur taxon sampling comprised 158 individuals (electronic supplementary material table S1 figure 1)including one Actenoides two Syma and 155 Todiramphus samples Of the 155 Todiramphus samples93 were T chloris and 62 were composed of 15 additional Todiramphus species We lacked only sixTodiramphus species (T diops T lazuli T albonotatus T funebris T enigma and T australasia) owing to theirdistribution in areas where collecting fresh genetic source material is difficult Our T chloris samplingincluded 22 of 50 nominal subspecies [29] Moyle [31] showed that Todiramphus is a clade distinct fromHalcyon and sister to Syma therefore we used Actenoides hombroni Syma megarhyncha and Syma torotoroas outgroups to root trees Whenever possible we sequenced multiple individuals per population (ieper island) to guard against errors of misidentification mislabelling or sample contamination

32 DNA sequencing alignment and model selectionWe extracted genomic DNA from frozen or alcohol-preserved muscle tissue toepads of museumstudy skins or unvouchered blood samples (electronic supplementary material table S1) using a non-commercial guanidine thiocyanate method [32] For toepad extractions we used laboratory spaceseparate from other Todiramphus pre- and post-PCR products to minimize contamination risk [33] Weused unvouchered blood samples for taxa from remote islands in French Polynesia where collection ofvouchered specimen material was not possible owing to small population sizes of endangered species(eg Todiramphus gambieri electronic supplementary material table S1 [34]) We sequenced the entiresecond and third subunits of mitochondrial nicotinamide adenine dinucleotide dehydrogenase (hereafterND2 and ND3 respectively) and four nuclear gene regions the coiled-coil domain containing protein132 (CCDC132) the high mobility group protein B2 (HMGB2) the third intron of the Z-linked muscle-specific kinase gene (MUSK) and the fifth intron of the transforming growth factor β2 (TGFβ2) followingprotocols described in [35] We used the following external primers in PCR amplification and sequencingL5215 (ND2 [36]) and H6313 (ND2 [37]) L10755 and H11151 (ND3 [38]) CDC132L and CDC132H[39] HMG2L and HMG2H [39] MUSK-I3F and MUSK-I3R [40] and TGF5 and TGF6 [41] We modifiedexternal primers for CCDC132 and HMGB2 to better suit Todiramphus and we designed internal primersto amplify 200ndash250 bp fragments of toepad samples (electronic supplementary material table S2)

We assembled and aligned sequence contigs in GENEIOUS v 61 (Biomatters) constructed individualnuclear intron alignments by hand and checked them against an automated alignment in MUSCLE[42] We phased introns in DNASP [43] with output threshold of 07 using algorithms provided byPHASE [4445] We identified appropriate models of sequence evolution for each of the seven partitions(electronic supplementary material table S3) using Akaikersquos information criterion (AIC) as implementedin MRMODELTEST v 23 [46]

33 Phylogenetic analysisWe performed phylogenetic reconstruction on the total concatenated data on separate concatenatedmitochondrial DNA (mtDNA) and nuclear DNA (nDNA) and separately on each locus We performedmaximum-likelihood (ML) heuristic tree searches in GARLI v 20 [47] and Bayesian analysis (BA) inMRBAYES v 321 [48ndash50] implemented with BEAGLE [51] We partitioned all ML and BA analyses bycodon position for mtDNA and by gene for the nuclear introns To avoid local optima in GARLI we did250 independent searches each starting from a random tree We adjusted GARLIrsquos default parametersto terminate searches when no topological improvements were found after 100 000 generations(genthreshfortopoterm = 100 000) otherwise we used default settings We assessed statistical supportfor the ML topology with 1000 non-parametric bootstrap replicates [52] and generated a 50 majority-rule consensus tree in SUMTREES v 331 part of the DENDROPY v 3120 package [53] In MRBAYESwe did four independent Markov chain Monte Carlo (MCMC) runs of 25 million generations usingfour chains per run (nchains = 4) with incremental heating of chains (temp = 01) sampled every2500 generations We changed the default branch length prior to unconstrained with an exponentialdistribution for all partitioned analyses to avoid artificially long branches (prset applyto = (all)brlenspr = unconstrainedexponential(100) [54]) We assessed convergence of parameter estimates andtree splits in TRACER v 15 [55] and ARE WE THERE YET (AWTY [5657]) respectively We assessedtopology convergence between runs by the average standard deviation of split frequencies (ASDSF) and

vairsquo

Rarsquo

Figure1Mapillustrating

samplingoftheTodiramphuschlorisspeciescomplexusedinthis

studyCirclessquaresandtrianglesrepresentsamplingpointsforTchlorisTsanctusandother(non-Tchloris)ingrouptaxarespectively

Coloureddistributionscorrespondtothe11majorphylogeneticlineagesoftheTchlorisspeciescomplexandmatchthecolouredcladesintheinsetphylogenyTheinsettopologyisfromtheBEASTtree(figure3)withcladeslabelled

AndashGmatching

thosefromtheM

RBAYEStree(figure2)Pointsarenotscaled

tothenum

berofsampledindividuals

perlocality(thereaderisreferredtotheelectronicsupplem

entarymaterialtableS1fornum

bersofindividuals

sampled)

potential scale reduction factor We discarded an appropriate number of burn-in generations based onconvergence assessments of the ASDSF passing below 001 the remaining trees were summarized in a50 majority-rule consensus tree

34 Molecular dating and species delimitationWe estimated divergence time in BEAST v 175 [5859] implemented with BEAGLE [51] We includedtwo individuals per nominal subspecies for all Todiramphus taxa except T sanctus for which we includedonly known breeding populations (eg Australia New Zealand New Caledonia Solomon IslandsVanuatu and the Santa Cruz group electronic supplementary material table S1) We linked clock andtree models but nucleotide substitution models were unlinked We used MRMODELTEST to partitionthe data in the same way we did our MRBAYES analyses (electronic supplementary material tableS3) We used a birthndashdeath speciation process for the tree prior To test for clock-like evolution wecompared likelihoods of runs with a strict clock to those with a relaxed lognormal clock (UCLD)We failed to reject a strict molecular clock using a likelihood ratio test (p = 10) Additionally thecoefficient of variation frequency histogram of the ucldstd parameter abutted against zero when viewedin TRACER which is a symptom that the data cannot reject a strict molecular clock [60] We ran10 independent MCMC chains for 100 million generations and sampled every 20 000th generationWe examined burn-in and convergence diagnostics in TRACER burn-in values were specific to eachrun with at least 25 of samples discarded with some runs requiring up to 40 burn-in Lackingfossil calibration data for this group we relied on published rates of mtDNA sequence evolution tocalibrate our divergence dating analyses Substitution rate priors derived from ND2 substitution ratesfor Hawaiian honeycreepers were used (0024 and 0033 substitutions per site Myrminus1 [61]) We choseND2 because it is one of the fastest-evolving mitochondrial gene regions in birds [61] and it is usedwidely among avian systematists and phylogeographers We used a lognormal prior distribution forthe clockrate parameter with mean = 0029 and standard deviation = 025 Using a general substitutionrate from distantly related species is not ideal (eg kingfishers versus honeycreepers) but we notethat mtDNA substitution rates across birds cluster around this value [1962] Regardless these dateestimates can only be used as a rough guide to clade ages We used separate normally distributedsubstitution rate calibration priors for the three ND2 codon positions whereas the introns werescaled to the mtDNA rate priors ND3 was omitted from BEAST analyses to simplify mitochondrialrate calibrations

We examined species delimitation and diversification rates to objectively compare patterns ofdiversity in T chloris to other published phylogenies of rapid geographical radiations (eg Zosterops andErythropitta) We delimited species with a Bayesian implementation of the general mixed Yule-coalescentmodel implemented in the R package bGMYC [63] We used the ND2 data and followed the authorsrsquoparameter recommendations [mcmc = 50 000 burn-in = 40 000 thinning = 100] The GMYC model [64]is advantageous for single-locus datasets such as those generated by DNA barcodes or when the majorityof phylogenetic signal occurs in the mtDNA including rapid radiations like Todiramphus We calculateddiversification rates assuming a Yule process from the following formula [ln(N)ndashln(No)]T which usesinitial diversity (No = 2) extant diversity (N) and time (T) since origin of the crown clade [65]

4 Results41 Phylogenetic relationshipsTopologies inferred from multiple independent ML and BA runs were highly concordant MCMCchain stationarity was achieved in MRBAYES (ie the ASDSF remained less than 001) after 815 milliongenerations Individual nuclear gene trees were largely uninformative at this shallow scale but bothmtDNA genes (ND2 and ND3) provided good phylogenetic resolution No conflicting topologies werestrongly supported between individual gene tree analyses (results not shown)

The ingroup included all T chloris samples plus 10 additional Todiramphus species (figure 2 clade Aposterior probability (PP) = 10 bootstrap support (BS) = 100) We defined this focal clade inclusive of Tfarquhari because this circumscribed a suite of 11 closely related species subtended by a long internodethat separated them from all other Todiramphus taxa Multiple instances of sympatry exist within the focalclade including on Australia (n = 2 taxa plus two outgroup taxa) Palau (n = 2) the Solomon Islands(n = 2 plus 1 outgroup) the Santa Cruz group (n = 2) and Vanuatu (n = 2 figure 2)

002 substitutionssite

MRBAYES concatenated

T chloris manuae KUNHM 107630

T chloris manuae KUNHM 104154T chloris manuae KUNHM 104156

T chloris solomonis KUNHM 15921T chloris solomonis KUNHM 12834T chloris solomonis KUNHM 15922

T chloris collaris FMNM 358326

T chloris alberti UWBM 66038

T chloris nusae KUNHM 27793T chloris nusae KUNHM 27812

T recurvirostris KUNHM 104178

T recurvirostris KUNHM 104171T recurvirostris KUNHM 104172

T sanctus sanctus KUNHM 7557T sanctus sanctus KUNHM 7567

T sanctus sanctus UWBM 57468

T sanctus sanctus UWBM 62818T sanctus sanctus UWBM 72545T sanctus sanctus UWBM 68059

T chloris solomonis KUNHM 15926

T chloris collaris KUNHM 14447

Todiramphus nigrocyaneus KUNHM 5294 [NEW GUINEA]

Syma megarhyncha KUNHM 7143 [NEW GUINEA]Actenoides hombroni KUNHM 19212

Syma torotoro KUNHM 5215 [NEW GUINEA AND N AUSTRALIA]

T winchelli KUNHM 14453T winchelli KUNHM 14302

T winchelli FMNH 358323T pyrrhopygius ANWC 32904 [AUSTRALIA]

T macleayii ANWC 33585 [AUSTRALIA]

T leucopygius KUNHM 15901

T leucopygius AMNH DOT 6654

T chloris collaris KUNHM 13960T chloris collaris KUNHM 13971

T chloris teraokai KUNHM 23631

T chloris vitiensis KUNHM 24247T chloris vitiensis KUNHM 24248

T chloris eximius KUNHM 25219T chloris eximius KUNHM 25227

T chloris vitiensis KUNHM 26529

T chloris sordidus KUNHM 8589

T chloris amoenus UWBM 58743T chloris amoenus UWBM 58741

T chloris humii UWBM 67535T chloris humii UWBM 76183

T chloris humii UWBM 76211

T chloris laubmannianus UWBM 81948

T chloris chloris AMNH DOT 12606 [Sulawesi]

T chloris amoenus AMNH DOT 6588

T saurophagus saurophagus KUNHM 27804T saurophagus saurophagus UWBM 60204T saurophagus saurophagus UWBM 60326T saurophagus saurophagus UWBM 69666

T chloris albicilla KUNHM 22581 [SAIPAN]T chloris albicilla KUNHM 22591 [SAIPAN]

T chloris albicilla KUNHM 22611 [SAIPAN]

T chloris orii UWBM 85102 [ROTA]T chloris orii UWBM 85104 [ROTA]T chloris orii UWBM 85105 [ROTA]

T chloris nusae KUNHM 27857

T farquhari LSUMZ 45388T farquhari LSUMZ 45401

T ruficollaris UWBM 42791T ruficollaris UWBM 42806

T tutus atiu UWBM 42503T tutus atiu UWBM 42504

T tutus mauke UWBM 42603T tutus mauke UWBM 42604

T tutus tutus MHNG HH7-60T tutus tutus MHNG HH7-62

T veneratus veneratus MHNG PO2-88

T veneratus youngi MHNG HH7-77T veneratus youngi MHNG HH7-75

T gambieri gertrudae MHNG PO343

T godeffroyi MNHN 1822T godeffroyi MNHN 1823

T sanctus canacorum MNHN NC10

T chloris marinus KUNHM 26411T chloris marinus KUNHM 26410

T chloris marinus KUNHM 26408T chloris marinus KUNHM 26393T chloris marinus KUNHM 26383T chloris marinus KUNHM 26369T chloris marinus KUNHM 26348T chloris marinus KUNHM 26342T chloris marinus KUNHM 26338T chloris marinus KUNHM 26439

T chloris colonus SNZP TKP2003070

T chloris sacer UWBM 42904T chloris sacer UWBM 42841T chloris sacer UWBM 42835

T chloris pealei UWBM 89771

T chloris pealei KUNHM 104160

T chloris sordidus ANWC 33720T chloris sordidus ANWC 33719

T chloris sordidus ANWC 51462

T chloris colcloughi ANWC 44296

T chloris ornatus KUNHM 19404 [SANTA CRUZ GROUP SOLOMON ISLANDS]

T chloris teraokai KUNHM 23630T chloris teraokai KUNHM 23690

T sanctus sanctus KUNHM 19403

T sanctus cancorum MNHN NC83

T sanctus sanctus AMNH DOT 12594

T sanctus sanctus ANWC 54622

T sanctus sanctus ANWC 50292T sanctus sanctus ANWC 34659

T sanctus vagans KUNHM 14879

T cinnamominus pelewensis KUNHM 23651T cinnamominus pelewensis KUNHM 23662T cinnamominus pelewensis KUNHM 23674

T cinnamominus cinnamominus KUNHM 47548 [GUAM MARIANA ISLANDS]T cinnamominus reichenbachii KUNHM 40147 [POHNPEI MICRONESIA]

T sanctus sanctus LSUMZ 45812

T chloris santoensis B45831 [VANUATU]

T chloris colonus SNZP TKP2003089T chloris colonus SNZP TKP2003092

T chloris alberti UWBM 60296T chloris alberti UWBM 60188

T chloris alberti AMNH DOT6704

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

RENNELL SOLOMON ISLANDS

MAKIRA AND UGI SOLOMON ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

ndashbreeds AUSTRALIA NEW ZEALAND E SOLOMON ISLANDS NEW CALEDONIA

ndashsome populations migrate in austral winter north to N AUSTRALIA NEW GUINEA SOLOMON ISLANDS SUNDA SHELF

SINGAPORE

PHILIPPINES PALAU AND

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

Figure 2 Molecular phylogeny of the Todiramphus chloris species complex The tree is the Bayesian maximum consensus treefrom the concatenated partitioned analysis with full sampling (n= 158 tips) Node support is denoted as Bayesian posteriorprobabilitiesmaximum-likelihoodbootstrap support Branch lengthsofActenoidesand Symawere reduced to save space Lettered clades(AndashI) are discussed in the text

Clade A contained seven subclades (figure 2 clades BndashI) each with PP = 10 except clade F (PP =096) which includes T cinnamominus from Guam and Pohnpei and T recurvirostris from Samoa Ofthe 10 non-T chloris species in the focal clade clade C comprised five species endemic to EasternPolynesia T godeffroyi T ruficollaris T veneratus T gambieri and T tutus Clade D was sister to cladeC and comprised T chloris lineages from Central Polynesia inclusive of American Samoa Tonga Fiji

Vanuatu and the eastern Solomon Islands including Makira Ugi and Rennell Islands and the SantaCruz group

The placement of clades E and F was equivocal The three subspecies of T cinnamominus were splitbetween these clades rendering the species paraphyletic The Palau endemic T c pelewensis was thesole member of clade E whereas T c cinnamominus and T c reichenbachii island endemics of Guam andPohnpei respectively were sequentially sister to T recurvirostris itself an endemic of American SamoaClade G comprised T chloris lineages from Australia and Papua New Guinea plus T sanctus which wasembedded inside this clade Clade H comprised three genetically distinct lineages nominal T c chlorisfrom Sulawesi T c humii from Singapore and a clade that comprised multiple subspecies from Borneo tothe Philippines and Palau Finally clade I included lineages from such geographically disparate regionsas Melanesia and the Mariana Islands Todiramphus saurophagus was sister to T c albicilla + T c orii fromSaipan and Rota Mariana Islands The other half of clade I included T c nusae and T c alberti of theBismarck Archipelago and Solomon Islands respectively to the exclusion of the eastern Solomon Islands(Makira Ugi and Rennell clade D)

42 Divergence times diversification rates and species limitsTodiramphus diversified rapidly and recently The ND2 sequence divergence within the focal clade(clade A) was 22 (median ND2 uncorrected P distance between T farquhari and all remaining clade Ataxa) The maximum pairwise divergence (34) occurred between the Southeast Asian clade includingnominate T c chloris (clade H) and the eastern Polynesian clade (clade C) We used two rates of ND2sequence divergence derived from the 95 CI range from Hawaiian honeycreeper mitogenomes (0024and 0033 substitutions per site Myrminus1 [61]) to calibrate the clock prior in our BEAST analysis Thefaster rate (33) results in a younger age estimate whereas the slower rate results in an older estimateThese calibrations place the start of diversification of clade A in the mid-Pleistocene approximately 057ndash085 Myr ago (mean 071 Ma figure 3) We caution against strict interpretation of these values becausedivergence time estimation based on a molecular clock has numerous shortcomings especially whenbased on single-gene calibrations from distantly related species as well as in the absence of fossil orisland-age calibrations

Threshold species delimitation with bGMYC suggested that current species diversity is vastlyunderestimated in Todiramphus Current taxonomic authorities [29] recognize 11 biological species thatare nested within our clade A The bGMYC estimate based on ND2 data only found strong supportfor 26 species within clade A plus seven species outside it (ie outgroup taxa figure 3) This estimateof 26 ingroup species probably is conservative because we lacked 28 of the 50 nominal subspecies ofT chloris We calculated two pairs of diversification rates based on estimates of species diversity inclade A the more conservative 11 lsquobio-speciesrsquo (eg following current taxonomy [29]) and our moreliberal bGMYC estimate of 26 ingroup species For each ingroup species scenario (11 and 26 speciesrespectively) we calculated diversification rates based on the range of crown clade ages derived from theBEAST divergence time estimation (057ndash085 Myr ago) Thus our conservative estimate (n = 11 ingroupspecies) yields a diversification rate of 201ndash299 sp Myrminus1 whereas our bGMYC-based estimate (n = 26ingroup species) is 302ndash449 sp Myrminus1 which surpasses the fastest speciation rates yet reported in birds[66] If we achieved complete taxon sampling of all 50 T chloris nominal subspecies our diversificationrate estimate probably would be higher

5 Discussion51 Timing and rates of diversificationPhylogenetic results indicate that characterization of T chloris as a lsquogreat speciatorrsquo [26] was notquite accurate because T chloris is not a natural group Indeed the reality is even more striking10 species were found to be embedded within or minimally divergent from T chloris renderingit paraphyletic Unbeknownst to Diamond et al [26] in their description of the paradox of thegreat speciators rapid geographical diversification of the T chloris complex was accompaniedby several instances of secondary sympatry involving morphologically disparate taxa (figure 3)which obscured their evolutionary relationships Phylogenetic reconstruction and molecular datingestimates revealed that the T chloris complex is extremely young and reached its geographicaldistribution quite rapidly The divergence between T farquhari and the rest of the ingroup wasonly 22 (ND2 uncorrected P) which yielded a crown clade divergence time estimate for the

T veneratus youngiT v veneratusT veneratus youngiT gambieri gertrudae

T tutus tutusT tutus atiu

T tutus mauke

T chloris santoensis

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T cinnamominus pelewensis

T cinn cinnamominusT cinn reichenbachii

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris collarisT chloris collarisT chloris laubmannianusT chloris nusaeT chloris nusaeT chloris albertiT chloris alberti

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T pyrrhopygiusT macleayii

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T chloris sordidusT chloris sordidusT chloris sordidusT chloris sordidus

T sanctus vagansT sanctus canacorum

T sanctus canacorum

T sanctus vagansT sanctus sanctusT sanctus sanctusT sanctus sanctusT sanctus sanctusT sanctus sanctus

T chloris colonus

T chloris manuaeT chloris manuaeT chloris pealei

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

teraokaipelewensis leucopygius

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Figure 3 Time-calibratedmaximumclade credibility treewith 95highest posterior density bars from theBEAST analysis Node supportis given as Bayesian posterior probability (PP) black circles at nodes denote PP= 10 grey circles denote 095le PPle 099 Unlabellednodes denote PPlt 095 The red vertical line denotes the bGMYC species delimitation estimate (ie the bGMYC analysis identified asspecies all clades to the right of the line) Sympatric lineages are identified by colour-coded labels that correspond to their respectivedistributions on the map Note that T sanctus is distributed across two coloured areas (green Australia and orange Solomon Islands)Actenoides hombroni Syma and Todiramphus nigrocyaneus were removed from the base of the tree to save space Lettered clades (AndashI)are discussed in the text and correspond to the same clades in figure 2 Illustrations of the sampled lineages from Palau (T c teraokai)and Vanuatu (T c santoensis) were not available so representative taxa from their respective clades were used (T c chloris and T c juliaerespectively) Illustrations courtesy of the Handbook of the Birds of the World Lynx Edicions

complex between 057 and 085 Ma This time frame in the mid-Pleistocene is more recent than thediversification of the red-bellied pitta Erythropitta erythrogaster throughout the Philippines Wallaceaand New Guinea (approx 18 Ma [10]) However we caution against drawing specific conclusionsbased on these time estimates because of myriad shortcomings of molecular clock calibrations fordivergence time estimation [67ndash69] Nevertheless our estimates of divergence time and species-level

diversity (ie unique evolutionary lineages) produced high diversification rate estimates comparedwith other birds [70] Overall we interpret the striking pattern of shallow internodes at thebase and relatively shallow divergences between ingroup taxa as support for a scenario in whichTodiramphus achieved its full geographical distributionmdashfrom French Polynesia to the Sunda Shelf(and possibly the Red Sea although those populations were not sampled)mdashrapidly and recentlySimilar patterns have been noted in other Pacific bird lineages including Acrocephalus reed-warblers[71] Alopecoenas doves [7273] Ceyx kingfishers [11] Erythropitta pittas [10] Pachycephala whistlers[3574] and Zosterops white-eyes [66] However not all Pacific bird lineages fit this pattern ofrapid and widespread diversification monarch flycatchers [7] and Ptilinopus fruit-doves [75] are twoexamples of widespread lsquomaturersquo lineages that have been diversifying throughout the Pacific formuch longer

52 Secondary sympatry shifting dispersal ability and migrationReduction in dispersal ability or propensity after geographical expansion is a leading hypothesis fordiversification of rapid geographical radiations in island settings [62676] Although rapid reductionof dispersal ability would allow for differentiation among island populations it would seeminglyprevent secondary colonization that is required to achieve sympatry This key evolutionary junctureis where the paradox of the great speciators [26] and the taxon cycles hypothesis [6] intersecttogether these hypotheses allow for differentiation and build-up of secondary sympatry with repeatedcolonization Among insular avian radiations a clear dichotomy exists between lineages that underwentexpansive geographical differentiation but rarely or never attained secondary sympatry [10113574]and those that display both broad geographical diversification as well as build-up of sympatric diversity[7131575] This can be seen in the Ceyx lepidus species complex (Aves Alcedinidae) which hasgeographical replacement populations across approximately 5000 km of the southwest Pacific but hasonly attained sympatry with close relatives in portions of the Philippines [11] Like Todiramphus thephylogeny of C lepidus has shallow internodes at the base with long branches subtending extant islandpopulations This pattern is consistent with rapid geographical expansion followed by reduction indispersal ability across all of C lepidus Based on our molecular dates C lepidus is about twice asold as the entire T chloris radiation Clade age can affect interpretation of diversification rate [7778]but it appears that C lepidus is a lineage whose diversification slowed after an initial stage of rapidgeographical expansion

Reduction in dispersal propensity however need not proceed uniformly across a clade Indeed railsPtilinopus fruit-doves and Zosterops white-eyes show marked differences in dispersal ability amongclosely related lineages across the Pacific [667579ndash81] Importantly all three groups also have substantialsecondary sympatry among species (rails did prior to widespread extinction) which coincides withdispersive taxa Wilson [82] noted the possibility of this uneven change in dispersal ability within adiversifying lineage in the context of cyclic expansion and contraction phases in diversification Thelayering of Todiramphus taxa resulting from such cycles is best illustrated in the Solomon Islands FourTodiramphus species breed on the larger islands and are clearly differentiated by age habitat and inferreddispersal propensity (figure 3)

In the context of Diamondrsquos [26] and Wilsonrsquos [6] views on the influence of variable dispersal abilitieson diversification patterns the T chloris complex contains multiple instances of secondary sympatry thatjuxtapose taxa with markedly different dispersal histories The incidence of secondary sympatry acrossthe Pacific distribution of the T chloris group is remarkably high given the recency of the radiation Inevery case the sympatric lineages diverged substantially in terms of phenotype morphology ecologydispersal abilitypropensity andor behaviour For example Palau holds two Todiramphus speciesT cinnamominus pelewensis and T chloris teraokai These taxa have diverged morphologically and in habitatpreference such that T c pelewensis is ca 50 smaller in body mass and inhabits forest interior whereasT chloris teraokai is larger and prefers coconut groves and beaches [3083] The species differ in plumageas well T c pelewensis has an orange crown whereas T chloris teraokai has a blue-green crown typicalof many T chloris forms A difference in dispersal history can be inferred from distributions and geneticstructure of the two taxa T c pelewensis is restricted to the Palau Archipelago and a relatively largegenetic divergence separates it from its nearest relative By contrast T chloris teraokai is embedded in arelatively undifferentiated clade that also spans the Philippine archipelago and Borneo It appears thatPalau was first colonized by T cinnamominus with T chloris arriving quite recently (figure 3) This nestedpattern of old and young lineages within an archipelago was also noted recently in Ptilinopus fruit-dovesfrom Fiji and Tonga [75]

The beach kingfisher Todiramphus saurophagus which is broadly sympatric with the T chloris clade

from the Bismarck Archipelago and Solomon Islands displays a similar pattern Todiramphus saurophagusis the largest species in the genus it is twice the size of the sympatric T chloris forms and it differsphenotypically from most other Todiramphus in having a completely white head (save a blue post-ocularstripe) It inhabits beaches coastal forest reefs islets and occasionally mangroves but never venturesfar from the coast Throughout its distribution from the northern Moluccas to the Solomon Islands it issympatric with one to two species of Todiramphus including representative T chloris forms For exampleT chloris alberti and T chloris nusae occur in the Solomon Islands and Bismarck Archipelago respectivelywhere they inhabit secondary forest and open areas away from the coast Notably T saurophagus andboth T chloris subspecies are in the same subclade of the T chloris phylogeny and diverged from oneanother quite recently perhaps 05 Ma (figure 3)

The most complex scenario of secondary sympatry in Todiramphus occurs in clade G (figure 2) Thisclade comprises all T chloris from Australia and New Guinea which are split in two lineages (i) anendemic to the Milne Bay Province islands of southeast Papua New Guinea T c colonus and (ii) theAustralian clade T c sordidus + T c colcloughi These allopatric lineages occur in different habitatsforest edge on small islands in the DrsquoEntrecasteaux and Louisiade Archipelagos (T c colonus) andmangrove forest and coastal estuaries of northern and eastern Australia (T c sordidus + T c colcloughi)Todiramphus sanctus is the third lineage in clade G This species is widespread and some populationsare highly migratory Its breeding range spans Australia New Zealand New Caledonia and parts ofthe Solomon Islands Many populations migrate north in the austral winter to the Sunda Shelf NewGuinea and Northern Melanesia We sampled three of the five nominal subspecies [29] including twofrom previously unknown localities (Nendo Island Santa Cruz group and Espiritu Santo Vanuatu)and despite the geographical complexity of this speciesrsquo distribution there was no genetic substructurewithin T sanctus individuals from migratory and sedentary populations across their broad distributionare intermixed in the clade

Sympatric forms of T chloris and T sanctus differ ecomorphologically and behaviourally Todiramphussanctus is smaller than any sympatric T chloris throughout its range Behaviourally the migratory natureof T sanctus is novel in Todiramphus kingfishers This behaviour is particularly relevant in light of thelsquogreat speciatorsrsquo paradox [26] The paradox poses the question why are some species geographicallywidespread implying high dispersal ability but at the same time well-differentiated across even narrowwater gaps implying low dispersal ability Diamond et al [26] suggested that some of the lsquogreatspeciatorsrsquo underwent colonization cycles in which they had past phases of higher immigration rates anddispersal abilities followed by a loss of dispersal ability with subsequent differentiation on newfoundislands They count Todiramphus [Halcyon] chloris among the several lineages as evidence for this ideaThat the migratory T sanctus is so closely related to T chlorismdashespecially given its placement deeplyembedded in the phylogenymdashemphasizes the potential role of shifts in dispersal ability as a driver ofdiversification It is possible that the migratory nature of T sanctus is an evolutionary vestige of theancestral Todiramphus lineage still exhibiting the colonization phase of Diamond et al [26] If so T sanctusoffers intriguing evidence in support of this component of the paradox

Rapid reduction of dispersal ability in island birds has been suspected [668485] and evidencesuggests that morphological change is not necessary for such a shift in dispersal ability it can be entirelybehavioural [86] It has also been shown that birds can acquire migratory ability quickly in response toselective pressure [8788] and this trait is thought to be evolutionarily labile [89] A prevailing paradigmis that extant migratory species evolved from sedentary tropical ancestors [90] however recent evidencein emberizoid passerines suggests otherwise [9192] Loss of migration may be as common as gains andextant sedentary tropical radiations (eg some Geothlypis and a clade containing Myiothlypis Basileuterusand Myioborus) represent at least two losses of latitudinal migration with possible colonization of thetropics from the temperate region [91]

6 ConclusionEarly biogeographers such as Darwin Wallace and Darlington appreciated that lineages can diversifyacross vast insular systems Subsequent observation led to description of similar patterns acrossmany of these radiations and formulation of hypotheses to explain them (eg lsquoTaxon Cyclesrsquo andlsquoGreat Speciatorsrsquo) We showed that the T chloris group exhibits three characteristics of particularinterest in discussions of how diversity accumulates on islands First the group diversified rapidlyconcomitant with a geographical expansion covering approximately 16 000 km of longitude This

diversification rate is among the most rapid known in birds [6670] Second within the shorttime frame of diversification secondary sympatry has been achieved multiple times Although it isunmeasured in many groups a broad survey of times to secondary sympatry in New World birds[19] reveals that T chloris is exceptional in its short time to secondary sympatry Third extremedisparity in dispersal ability has evolved within the groupmdashmigratory T sanctus is embedded withinthe sedentary T chloris complex Together these aspects support a hypothesis that rapid and unevenshifts in dispersal propensity across clades have been prominent in moulding the evolution ofinsular biotas

Ethics statement This project operated under IACUC approval AUS no 174-01 issued to RGM at the University ofKansasData accessibility All DNA sequences generated in this study are deposited in GenBank under accession numbers(KP291162ndashKP292029)Acknowledgements We are grateful to the following collections managers and curators for providing loans of tissue ortoepad samples from their institutions Paul Sweet Peter Capainolo Tom Trombone and Joel Cracraft AmericanMuseum of Natural History Robert Palmer and Leo Joseph Australian National Wildlife Collection AndrewKratter and David Steadman University of Florida Museum of Natural History Donna Dittmann LouisianaState University Museum of Natural Science Mark Robbins University of Kansas Biodiversity Institute EricPasquet Museacuteum National drsquoHistoire Naturelle Paris Rob Fleischer Smithsonian National Zoological ParkSharon Birks University of Washington Burke Museum MJA and RGM thank Alivereti Naikatini MarikaTuiwawa Mika Bolakania Sanivalati Vido Lulu Cakacaka and Joeli Vakabua for assistance with permits andfieldwork in Fiji the Department of Environment and Conservation NRI (Georgia Kaipu) and PNGIBR (MiriamSupuma) for assistance and permission to work in Papua New Guinea the Ministry of Environment ClimateChange Disaster Management and Meterology in Solomon Islands Protected Areas and Wildlife Bureau ofthe Philippine Department of Environment and Natural Resources CNMI Division of Fish amp Wildlife (PaulRadley) in the Mariana Islands and Belau National Museum (Allan Olsen) Division of Fish and WildlifeProtection (Kammen Chin) Bureau of Agriculture (Fred Sengebau Gwen Bai and Hilda Etpison) and theKoror State Office (Hulda Blesam) in Palau AC and J-CT thank Jean-Yves Meyer (Research delegation of theGovernment of French Polynesia) Philippe Raust (Socieacuteteacute drsquoOrnithologie de Polyneacutesie) Claude Serra (Directionde lrsquoEnvironnement French Polynesia) and the Institut pour la Recherche et le Deacuteveloppement (IRD Tahiti) fortheir help and support during fieldwork in French Polynesia We are grateful to Lynx Edicions for permissionto use illustrations from the Handbook of the Birds of the World series (illustrated by Norman Arlott) Helpfulcomments were provided by Brian T Smith H Douglas Pratt Thane Pratt Matthew L Knope and oneanonymous reviewerAuthorsrsquo contributions MJA and RGM conceived the design of this project MJA AC J-CT CEF and RGMconducted fieldwork MJA HTS and AC carried out the molecular laboratory work and sequence alignmentsMJA conducted the data analysis and drafted the manuscript together with RGM All authors participated inediting the manuscript and all authors gave final approval for publicationFunding statement This project was funded in part by an American Museum of Natural History Chapman Fellowship(MJA) an American Ornithologistsrsquo Union Research Award (MJA) a University of Kansas Doctoral StudentResearch Fund (MJA) and NSF DEB-1241181 and DEB-0743491 (RGM)Competing interests The authors claim no competing interests in this work

References1 Mayr E 1942 Systematics and the origin of species

New York NY Columbia University Press2 Mayr E Diamond J 2001 The birds of Northern

Melanesia speciation ecology and biogeographyNew York NY Oxford University Press

3 Diamond JM 1977 Continental and insularspeciation in Pacific land birds Syst Zool 26263ndash268 (doi1023072412673)

4 Lack D 1947 Darwinrsquos finches Cambridge UKCambridge University Press

5 MacArthur RH Wilson EO 1967 The theory of islandbiogeography Princeton NJ Princeton UniversityPress

6 Wilson EO 1961 The nature of the taxon cycle in theMelanesian ant fauna Am Nat 95 169ndash193(doi101086282174)

7 Filardi CE Moyle RG 2005 Single origin of apan-Pacific bird group and upstream colonization of

Australasia Nature 438 216ndash219(doi101038nature04057)

8 Daacutevalos LM 2007 Short-faced bats (PhyllostomidaeStenodermatina) a Caribbean radiation of strictfrugivores J Biogeogr 34 364ndash375(doi101111j1365-2699200601610x)

9 Hutsemeacutekers V Szoumlveacutenyi P Shaw AJGonzaacutelez-Mancebo J-M Muntildeoz J Vanderpoorten A2011 Oceanic islands are not sinks of biodiversity inspore-producing plants Proc Natl Acad Sci USA108 18 989ndash18 994 (doi101073pnas1109119108)

10 Irestedt M Fabre P-H Batalha-Filho H Joslashnsson KARoselaar CS Sangster G Ericson PGP 2013 Thespatio-temporal colonization and diversificationacross the Indo-Pacific by a lsquogreat speciatorrsquo (AvesErythropitta erythrogaster) Proc R Soc B 28020130309 (doi101098rspb20130309)

11 Andersen MJ Oliveros CH Filardi CE Moyle RG 2013Phylogeography of the variable dwarf-kingfisherCeyx lepidus (Aves Alcedinidae) inferred frommitochondrial and nuclear DNA sequences Auk 130118ndash131 (doi101525auk201212102)

12 Uy JAC Moyle RG Filardi CE 2009 Plumage andsong differences mediate species recognitionbetween incipient flycatcher species of the SolomonIslands Evolution 63 153ndash164(doi101111j1558-5646200800530x)

13 Nyaacuteri AacuteS Benz BW Joslashnsson KA Fjeldsaring J Moyle RG2009 Phylogenetic relationships of fantails (AvesRhipiduridae) Zool Scr 38 553ndash561(doi101111j1463-6409200900397x)

14 Andersen MJ Naikatini A Moyle RG 2014A molecular phylogeny of Pacific honeyeaters(Aves Meliphagidae) reveals extensive paraphylyand an isolated Polynesian radiationMol

Phylogenet Evol 71 308ndash315 (doi101016jympev201311014)

15 Joslashnsson KA Bowie RCK Nylander JAA Christidis LNorman JA Fjeldsaring J 2010 Biogeographical historyof cuckoo-shrikes (Aves Passeriformes)transoceanic colonization of Africa fromAustralo-Papua J Biogeogr 37 1767ndash1781(doi101111j1365-2699201002328x)

16 Gillespie R 2004 Community assembly throughadaptive radiation in Hawaiian spiders Science 303356ndash359 (doi101126science1091875)

17 Losos JB Ricklefs RE 2009 Adaptation anddiversification on islands Nature 457 830ndash836(doi101038nature07893)

18 Weeks BC Claramunt S 2014 Dispersal has inhibitedavian diversification in Australasian archipelagoesProc R Soc B 281 20141257 (doi101098rspb20141257)

19 Weir JT Price TD 2011 Limits to speciation inferredfrom times to secondary sympatry and ages ofhybridizing species along a latitudinal gradientAm Nat 177 462ndash469 (doi101086658910)

20 Tobias JA Cornwallis CK Derryberry EP ClaramuntS Brumfield RT Seddon N 2013 Species coexistenceand the dynamics of phenotypic evolution inadaptive radiation Nature 506 359ndash363(doi101038nature12874)

21 Ricklefs RE 2010 Evolutionary diversificationcoevolution between populations and theirantagonists and the filling of niche space Proc NatlAcad Sci USA 107 1265ndash1272 (doi101073pnas0913626107)

22 Ricklefs RE 2010 Hostndashpathogen coevolutionsecondary sympatry and species diversificationPhil Trans R Soc B 365 1139ndash1147(doi101098rstb20090279)

23 Peterson AT Soberoacuten J Saacutenchez-Cordero V 1999Conservatism of ecological niches in evolutionarytime Science 285 1265ndash1267(doi101126science28554311265)

24 Pigot AL Tobias JA 2013 Species interactionsconstrain geographic range expansion overevolutionary time Ecol Lett 16 330ndash338(doi101111ele12043)

25 Tobias JA Planqueacute R Cram DL Seddon N 2014Species interactions and the structure of complexcommunication networks Proc Natl Acad Sci USA111 1020ndash1025 (doi101073pnas1314337111)

26 Diamond JM Gilpin ME Mayr E 1976Species-distance relation for birds of the SolomonArchipelago and the paradox of the greatspeciators Proc Natl Acad Sci USA 73 2160ndash2164(doi101073pnas7362160)

27 Fry CH Fry K Harris A 1992 Kingfishers bee-eaters amprollers a handbook 324 p Princeton NJ PrincetonUniversity Press

28 Woodall PF 2001 Family Alcedinidae (kingfishers)In Handbook of the Birds of the World vol 6Mousebirds to hornbills (eds J del Hoyo A Elliott JSargatal) pp 130ndash249 Barcelona Spain LynxEdicions

29 Gill FB Donsker D 2014 IOC World Bird List (v43)See httpwwwworldbirdnamesorg

30 Fry CH 1980 The evolutionary biology of kingfishers(Alcedinidae) Living Bird 18 113ndash160

31 Moyle RG 2006 A molecular phylogeny ofkingfishers (Alcedinidae) with insights into earlybiogeographic history Auk 123 487ndash499(doi1016420004-8038(2006)123[487AMPOKA]20CO2)

32 Esselstyn JA Garcia HJD Saulog MG Heaney LR2008 A new species of Desmalopex (Pteropodidae)

from the Philippines with a phylogenetic analysisof the Pteropodini J Mammal 89 815ndash825(doi10164407-MAMM-A-2851)

33 Mundy NI Unitt P Woodruff DS 1997 Skin from feetof museum specimens as a non-destructive sourceof DNA for avian genotyping Auk 114 126ndash129(doi1023074089075)

34 Kesler DC Haig SM 2007 Conservation biology forsuites of species demographic modeling for Pacificisland kingfishers Biol Conserv 136 520ndash530(doi101016jbiocon200612023)

35 Andersen MJ Nyaacuteri AacuteS Mason I Joseph LDumbacher JP Filardi CE Moyle RG 2014 Molecularsystematics of the worldrsquos most polytypic bird thePachycephala pectoralismelanura (AvesPachycephalidae) species complex Zool J Linn Soc170 566ndash588 (doi101111zoj12088)

36 Hackett SJ 1996 Molecular phylogenetics andbiogeography of tanagers in the genusRamphocelus (Aves)Mol Phylogenet Evol 5368ndash382 (doi101006mpev19960032)

37 Johnson KP Sorenson MD 1998 Comparingmolecular evolution in two mitochondrial proteincoding genes (cytochrome b and ND2) in thedabbling ducks (Tribe Anatini)Mol PhylogenetEvol 10 82ndash94 (doi101006mpev19970481)

38 Chesser RT 1999 Molecular systematics of therhinocryptid genus Pteroptochos Condor 101439ndash446 (doi1023071370012)

39 Backstroumlm N Fagerberg S Ellegren H 2008Genomics of natural bird populations a gene-basedset of reference markers evenly spread across theavian genomeMol Ecol 17 964ndash980(doi101111j1365-294X200703551x)

40 Kimball RT et al 2009 A well-tested set of primers toamplify regions spread across the avian genomeMol Phylogenet Evol 50 654ndash660(doi101016jympev200811018)

41 Primmer CR Borge T Lindell J Saeligtre GP 2002Single-nucleotide polymorphism characterizationin species with limited available sequenceinformation high nucleotide diversity revealed inthe avian genomeMol Ecol 11 603ndash612(doi101046j0962-1083200101452x)

42 Edgar RC 2004 MUSCLE multiple sequencealignment with high accuracy and high throughputNucleic Acids Res 32 1792ndash1797(doi101093nargkh340)

43 Librado P Rozas J 2009 DNASP v5 a software forcomprehensive analysis of DNA polymorphism dataBioinformatics 25 1451ndash1452(doi101093bioinformaticsbtp187)

44 Stephens M Donnelly P 2003 A comparison ofBayesian methods for haplotype reconstructionfrom population genotype data Am J Hum Genet73 1162ndash1169 (doi101086379378)

45 Stephens M Smith NJ Donnelly P 2001 A newstatistical method for haplotype reconstructionfrom population data Am J Hum Genet 68978ndash989 (doi101086319501)

46 Nylander JAA 2004 MRMODELTEST v2 (Programdistributed by the author Evolutionary BiologyCentre Uppsala University

47 Zwickl DJ 2006 Genetic algorithm approaches for thephylogenetic analysis of large biological sequencedatasets under the maximum likelihood criterionAustin TX The University of Texas

48 Ronquist F Huelsenbeck JP 2003 MRBAYES 3Bayesian phylogenetic inference under mixedmodels Bioinformatics 19 1572ndash1574(doi101093bioinformaticsbtg180)

49 Altekar G Dwarkadas S Huelsenbeck JP Ronquist F2004 Parallel metropolis coupled Markov chainMonte Carlo for Bayesian phylogenetic inferenceBioinformatics 20 407ndash415(doi101093bioinformaticsbtg427)

50 Ronquist F et al 2012 MRBAYES 32 efficient Bayesianphylogenetic inference and model choice across alarge model space Syst Biol 61 539ndash542(doi101093sysbiosys029)

51 Ayres DL et al 2012 BEAGLE an applicationprogramming interface and high-performancecomputing library for statistical phylogenetics SystBiol 61 170ndash173 (doi101093sysbiosyr100)

52 Felsenstein J 1985 Confidence limits onphylogenies an approach using the bootstrapEvolution 39 783ndash791 (doi1023072408678)

53 Sukumaran J Holder MT 2010 DENDROPY a Pythonlibrary for phylogenetic computing Bioinformatics26 1569ndash1571 (doi101093bioinformaticsbtq228)

54 Brown JM Hedtke SM Lemmon AR Lemmon EM2010 When trees grow too long investigating thecauses of highly inaccurate Bayesian branch-lengthestimates Syst Biol 59 145ndash161(doi101093sysbiosyp081)

55 Rambaut A Drummond A 2007 TRACER v15 Seehttptreebioedacuksoftwaretracer

56 Nylander JAA Wilgenbusch JC Warren DL SwoffordDL 2008 AWTY (are we there yet) a system forgraphical exploration of MCMC convergence inBayesian phylogenetics Bioinformatics 24581ndash583 (doi101093bioinformaticsbtm388)

57 Wilgenbusch JC Warren DL Swofford DL 2004AWTY a system for graphical exploration of MCMCconvergence in Bayesian phylogenetic inferenceSee httpcebcsitfsueduawty

58 Drummond AJ Suchard MA Xie D Rambaut A 2012Bayesian phylogenetics with BEAUti and the BEAST17Mol Biol Evol 29 1969ndash1973(doi101093molbevmss075)

59 Drummond AJ Nicholls GK Rodrigo AG SolomonW 2002 Estimating mutation parameterspopulation history and genealogy simultaneouslyfrom temporally spaced sequence data Genetics161 1307ndash1320

60 Drummond AJ Ho SYW Rawlence N Rambaut A2007 A rough guide to BEAST 14 (retrieved 1 April2014) See httpworkshopmolecularevolutionorgmolevolfilesbeastBEAST14_MANUAL-7-6-07pdf

61 Lerner HR Meyer M James HF Hofreiter MFleischer RC 2011 Multilocus resolution ofphylogeny and timescale in the extant adaptiveradiation of Hawaiian honeycreepers Curr Biol 211838ndash1844 (doi101016jcub201109039)

62 Weir JT Bermingham E Miller MJ Klicka J GonzalezMA 2008 Phylogeography of a morphologicallydiverse Neotropical montane species the commonbush-tanager (Chlorospingus ophthalmicus)MolPhyl Evol 47 650ndash664(doi101016jympev200802004)

63 Reid NM Carstens BC 2012 Phylogenetic estimationerror can decrease the accuracy of speciesdelimitation a Bayesian implementation of thegeneral mixed Yule-coalescent model BMC EvolBiol 12 196 (doi1011861471-2148-12-196)

64 Pons J Barraclough T Gomez-Zurita J Cardoso ADuran D Hazell S Kamoun S Sumlin W Vogler A2006 Sequence-based species delimitation for theDNA taxonomy of undescribed insects Syst Biol 55595ndash609 (doi10108010635150600852011)

65 Magallon S Sanderson MJ 2001 Absolute

diversification rates in angiosperm clades Evolution55 1762ndash1780 (doi101111j0014-38202001tb00826x)

66 Moyle RG Filardi CE Smith CE Diamond JM 2009Explosive Pleistocene diversification andhemispheric expansion of a lsquogreat speciatorrsquo ProcNatl Acad Sci USA 106 1863ndash1868(doi101073pnas0809861105)

67 Lovette IJ 2004 Mitochondrial dating and mixedsupport for the lsquo2rsquo rule in birds Auk 121 1ndash6

68 Arbogast BS Edwards SV Wakeley J Beerli PSlowinski JB 2002 Estimating divergence timesfrommolecular data on phylogenetic andpopulation genetics timescales Annu Rev EcolSyst 33 707ndash740(doi101146annurevecolsys33010802150500)

69 Lanfear R Welch JJ Bromham L 2010 Watching theclock studying variation in rates of molecularevolution between species Trends Ecol Evol 25495ndash503 (doi101016jtree201006007)

70 Jetz W Thomas GH Joy JB Hartmann K Mooers AO2012 The global diversity of birds in space and timeNature 491 444ndash448 (doi101038nature11631)

71 Cibois A Beadell JS Graves GR Pasquet E Slikas BSonsthagen SA Thibault J-C Fleischer RC 2011Charting the course of reed-warblers across thePacific islands J Biogeogr 38 1963ndash1975(doi101111j1365-2699201102542x)

72 Moyle RG Jones RM Andersen MJ 2013 Areconsideration of Gallicolumba (Aves Columbidae)relationships using fresh source material revealspseudogenes chimeras and a novel phylogenetichypothesisMol Phylogenet Evol 66 1060ndash1066(doi101016jympev201211024)

73 Joslashnsson KA Irestedt M Bowie RCK Christidis LFjeldsaring J 2011 Systematics and biogeographyof Indo-Pacific ground-dovesMol Phylogenet

Evol 59 538ndash543 (doi101016jympev201101007)

74 Joslashnsson KA Irestedt M Christidis L Clegg SM HoltBG Fjeldsa J 2014 Evidence of taxon cycles in anIndo-Pacific passerine bird radiation (AvesPachycephala) Proc R Soc B 281 20131727(doi101098rspb20131727)

75 Cibois A Thibault J-C Bonillo C Filardi CE WatlingD Pasquet E 2014 Phylogeny and biogeography ofthe fruit doves (Aves Columbidae)Mol PhylogenetEvol 70 442ndash453 (doi101016jympev201308019)

76 Carlquist SJ 1974 Island biology ix 660 ppNew York NY Columbia University Press

77 Knope ML Morden CW Funk VA Fukami T 2012Area and the rapid radiation of Hawaiian Bidens(Asteraceae) J Biogeogr 39 1206ndash1216(doi101111j1365-2699201202687x)

78 Rabosky DL 2009 Ecological limits anddiversification rate alternative paradigms toexplain the variation in species richness amongclades and regions Ecol Lett 12 735ndash743(doi101111j1461-0248200901333x)

79 Bertrand JAM et al 2014 Extremely reduceddispersal and gene flow in an island bird Heredity112 190ndash196 (doi101038hdy201391)

80 Slikas B Olson SL Fleischer RC 2002 Rapidindependent evolution of flightlessness in fourspecies of Pacific Island rails (Rallidae) an analysisbased on mitochondrial sequence data J AvianBiol 33 5ndash14 (doi101034j1600-048X2002330103x)

81 Kirchman JJ 2012 Speciation of flightless rails onislands a DNA-based phylogeny of the typical railsof the Pacific Auk 129 56ndash69(doi101525auk201211259)

82 Wilson EO 1959 Adaptive shift and dispersal in atropical ant fauna Evolution 13 122ndash144(doi1023072405948)

83 Pratt HD Etpison MT 2008 Birds and bats of PalauHonolulu HI Mutual Publishing LLC

84 Olson SL 1973 Evolution of the rails of the SouthAtlantic islands (Aves Rallidae) Smithson ContribZool 152 1ndash53 (doi105479si00810282152)

85 Diamond JM 1981 Flightlessness and fear of flyingin island species Nature 293 507ndash508(doi101038293507a0)

86 Komdeur J Piersma T Kraaijeveld KKraaijeveld-Smit F Richardson DS 2004 WhySeychelles warblers fail to recolonize nearbyislands unwilling or unable to fly there Ibis 146298ndash302 (doi101046j1474-919X200400255x)

87 Berthold P Helbig AJ Mohr G Querner U 1992Rapid microevolution of migratory behaviour in awild bird species Nature 360 668ndash670(doi101038360668a0)

88 Helbig AJ 1994 Genetic basis and evolutionarychange of migratory directions in a Europeanpasserine migrant Sylvia atricapilla Ostrich 65151ndash159 (doi1010800030652519949639677)

89 Pulido F 2007 The genetics and evolution of avianmigration BioScience 57 165ndash174(doi101641B570211)

90 Gauthreaux SA 1982 The ecology and evolution ofavian migration systems In Avian biology (eds DSFarner JR King KC Parkes) pp 93ndash168 New YorkNY Academic Press

91 Winger BM Lovette IJ Winkler DW 2012 Ancestryand evolution of seasonal migration in theParulidae Proc R Soc B 279 610ndash618(doi101098rspb20111045)

92 Winger BM Barker FK Ree RH 2014 Temperateorigins of long-distance seasonal migration in NewWorld songbirds Proc Natl Acad Sci USA 11112 115ndash12 120 (doi101073pnas1405000111)

Summary

Introduction

Material and methods

Taxon sampling

DNA sequencing alignment and model selection

Phylogenetic analysis

Molecular dating and species delimitation

Results

Phylogenetic relationships

Divergence times diversification rates and species limits

Discussion

Timing and rates of diversification

Secondary sympatry shifting dispersal ability and migration

Conclusion

References

from Polynesian taxa In light of our results we discuss systematic relationships of Todiramphus andpropose an updated taxonomy This paper contributes to our understanding of avian diversification andassembly on islands and to the systematics of a classically polytypic species complex

2 IntroductionClassic hypotheses about diversification of insular organisms are based on a relatively simple dynamicbetween colonization and extinction of allopatrically derived species [1ndash6] These ideas are beingchallenged however by phylogenies that support complex diversification and colonization scenarios(eg [7ndash9]) This re-evaluation of insular diversification has revealed extensive insular radiations withhigh sympatric diversity and subsequent re-colonization of continental areas Thus community diversityon islands depends not only on the flow of colonists from continental areas but also on the frequencyof secondary sympatry within insular lineages Furthermore a broad spectrum of lineage ages existsin island systems For example recent phylogenetic study has uncovered the ubiquity of insular avianlineages exhibiting recent allopatric diversification over large areas of the Pacific [10ndash12] providing acontext for high potential speciation rates Conversely lsquomaturersquo insular radiations exist with extensive co-occurrence of constituent taxa and substantial ecomorphological differentiation which often confoundedtraditional taxonomy [712ndash15]

The rate of attaining reproductive isolation and the build-up of sympatry (ie assembly) on islands isunderstudied in non-adaptive radiations (eg away from Hawaii and the Galaacutepagos [16ndash18]) A keycomponent is the critical stage after initial geographical expansion and subsequent diversification(ie allopatric speciation) when diversifying lineages initiate secondary sympatry among recentlydiverged populations Unfortunately most avian radiations are not suitable for studying the processof secondary sympatry on islands For example mature insular radiations provide only an incompletepicture because extinction changes in distribution and substantial anagenesis obscures early stagesof lineage accumulation whereas purely geographical radiations (eg [10]) have not yet begunthe process thus they are uninformative in the study of insular species assembly and secondarysympatry Evidence from mature continental radiations supports a scenario of substantial divergencein allopatry before lineages are able or have the opportunity to co-occur [1920] however factorsthat influence rates to secondary sympatry in continental systems are numerous complex geographyclosed ecological communities disease transmission biotic and abiotic environmental interactionsecological similarity of sister taxa and complex signalling environments [20ndash25] Conversely insularsystems are comparatively simple and may provide the most accessible insight into the tempo andmode of attaining secondary sympatry even though extrapolation to diverse continental systems isdifficult [17]

Here we examine the phylogeographic and temporal patterns of diversification in the Todiramphuschloris species complex (Aves Alcedinidae) and its close relatives This species complex is the mostwidespread of the archetypal lsquogreat speciatorsrsquo [26] and comprises 50 nominal subspecies spanninga distance more than 16 000 km from the Red Sea to Samoa [27ndash29] The full geographical extent ofthe genus extends a further 3000 km east to the Marquesas Islands in Eastern Polynesia (kingfishersdo not occur in Hawaii) Most nominal subspecies correspond to single-island populations that arephenotypically distinct in plumage and size but some islandsarchipelagos have multiple sympatricTodiramphus species including Palau Vanuatu and several islands in the Solomon Islands andthe Bismarck Archipelago as well as Australia These instances of sympatry are presumed to besecondary (ie after allopatric speciation) Additionally the distribution of Todiramphus sanctusmdashtheonly migratory Todiramphusmdashbroadly overlaps many congeners in the T chloris complex All sympatricTodiramphus exhibit ecological morphological and behavioural differences including separation byhabitat preference suggesting a high degree of reproductive isolation between each pair [272830]Previous phylogenetic work on higher level kingfisher relationships showed extremely low geneticdifferentiation among five Todiramphus species [31] but only one T chloris sample was included Withregard to non-adaptive (eg geographical) insular radiations the T chloris complex has several notablefeatures The broad distribution numerous instances of closely related sympatric species and closerelationship between migratory and sedentary species make the T chloris complex an ideal lineage forexamining the consequence of rapid diversification and subsequent assembly of secondarily sympatricspecies in an insular system

vairsquo

Rarsquo

AndashGmatching

thosefromtheM

tothenum

bersofindividuals

sampled)

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

SINGAPORE

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

vairsquo

Rarsquo

AndashGmatching

thosefromtheM

tothenum

bersofindividuals

sampled)

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

SINGAPORE

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

vairsquo

Rarsquo

AndashGmatching

thosefromtheM

tothenum

bersofindividuals

sampled)

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

SINGAPORE

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

SINGAPORE

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

1010010100

10861086

10ndash

099ndash

061ndash

096ndash

052ndash

10761094

097ndash

098ndash

096ndash

PHILIPPINES

SOCIETY AND

COOK ISLANDS

AMERICAN SAMOA

SOLOMON ISLANDS

VANUATU

MARQUESAS ISLANDS

LOUISIADE AND

DrsquoENTRECASTEAUX

AUSTRALIA

SINGAPORE

BORNEO

BISMARCK ARCH AND

SOLOMON ISLANDS

MARIANA ISLANDS

BISMARCK ARCH

SOLOMON ISLANDS

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

T tutus mauke

T chloris amoenus

T chloris solomonis

T chloris ornatus

T chloris sacer

T recurvirostris

T chloris chloris

T chloris humii

T saurophagus

T chloris albicilla

T chloris orii

T chloris teraokai

T chloris eximius

T chloris vitiensis

T chloris marinus

T chloris pealei

T winchelli

T leucopygius

T farquhari

T godeffroyi

T ruficollaris

T sanctus canacorum

T chloris colonus

05 Ma1015202530

Vanuatu

Solomon Islands

Australia

alberti

saurophagus

sanctussanctus

farquhari

santoensis

macleayiisordidus

pyrrhopygius

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Summary

Introduction

Taxon sampling




Results



Discussion



Conclusion

References

Documents

rsos.royalsocietypublishing.org Australo ...rsos.royalsocietypublishing.org/content/royopensci/2/2/140375.full.pdf · chloris species complex (Aves: Alcedinidae) and its close relatives