R Soc Open Sci R Soc Open Sci 2753 rsos 101647528 RSOS Royal Society Open Science 2054-5703 The Royal Society PMC4448819 PMC4448819.1 4448819 4448819 26064600 10.1098/rsos.140375 rsos140375 1 1001 70 183 Biology (Whole Organism) Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus ) Rapid diversification in kingfishers Andersen Michael J. 1 † Shult Hannah T. 1 ‡ Cibois Alice 2 Thibault Jean-Claude 3 Filardi Christopher E. 4 † Moyle Robert G. 1 1 Department of Ecology and Evolutionary Biology and Biodiversity Institute , University of Kansas , Lawrence, KS 66045, USA 2 Natural History Museum of Geneva, Department of Mammalogy and Ornithology , CP 6434, CH-1211 Geneva 6, 6434, Switzerland 3 Muséum National d'Histoire Naturelle, Département Systématique et Evolution , UMR7205, Case Postale 51, 55 Rue Buffon, 75005 Paris, France 4 American Museum of Natural History, Center for Biodiversity and Conservation , Central Park West at 79th Street, New York, NY 10024, USA Author for correspondence: Michael J. Andersen e-mail: mandersen@amnh.org † Present address: American Museum of Natural History, Department of Ornithology, Central Park West at 79th Street, New York, NY 10024, USA. ‡ Present address: Department of Entomology, Life Sciences Building, Louisiana State University, Baton Rouge, LA 70803, USA. 2 2015 4 2 2015 2 2 253541 140375 14 10 2014 6 1 2015 04 02 2015 10 06 2015 09 07 2023 © 2015 The Authors. 2015 https://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ , which permits unrestricted use, provided the original author and source are credited. Todiramphus chloris is the most widely distributed of the Pacific's ‘great speciators’. Its 50 subspecies constitute a species complex that is distributed over 16 000 km from the Red Sea to Polynesia. We present, to our knowledge, the first comprehensive molecular phylogeny of this enigmatic radiation of kingfishers. Ten Pacific Todiramphus species are embedded within the T. chloris complex, rendering it paraphyletic. Among these is a radiation of five species from the remote islands of Eastern Polynesian, as well as the widespread migratory taxon, Todiramphus sanctus . Our results offer strong support that Pacific Todiramphus , including T. chloris , underwent an extensive range expansion and diversification less than 1 Ma. Multiple instances of secondary sympatry have accumulated in this group, despite its recent origin, including on Australia and oceanic islands in Palau, Vanuatu and the Solomon Islands. Significant ecomorphological and behavioural differences exist between secondarily sympatric lineages, which suggest that pre-mating isolating mechanisms were achieved rapidly during diversification. We found evidence for complex biogeographic patterns, including a novel phylogeographic break in the eastern Solomon Islands that separates a Northern Melanesian clade from Polynesian taxa. In light of our results, we discuss systematic relationships of Todiramphus and propose an updated taxonomy. This paper contributes to our understanding of avian diversification and assembly on islands, and to the systematics of a classically polytypic species complex. island biogeography diversification rates divergence time estimation great speciators Todiramphus chloris pmc-status-qastatus 0 pmc-status-live yes pmc-status-embargo no pmc-status-released yes pmc-prop-open-access yes pmc-prop-olf no pmc-prop-manuscript no pmc-prop-legally-suppressed no pmc-prop-has-pdf yes pmc-prop-has-supplement yes pmc-prop-pdf-only no pmc-prop-suppress-copyright no pmc-prop-is-real-version no pmc-prop-is-scanned-article no pmc-prop-preprint no pmc-prop-in-epmc yes pmc-license-ref CC BY cover-date February, 2015 2. Introduction Classic hypotheses about diversification of insular organisms are based on a relatively simple dynamic between colonization and extinction of allopatrically derived species [ 1 – 6 ]. These ideas are being challenged, however, by phylogenies that support complex diversification and colonization scenarios (e.g. [ 7 – 9 ]). This re-evaluation of insular diversification has revealed extensive insular radiations with high sympatric diversity and subsequent re-colonization of continental areas. Thus, community diversity on islands depends not only on the flow of colonists from continental areas, but also on the frequency of secondary sympatry within insular lineages. Furthermore, a broad spectrum of lineage ages exists in island systems. For example, recent phylogenetic study has uncovered the ubiquity of insular avian lineages exhibiting recent, allopatric diversification over large areas of the Pacific [ 10 – 12 ], providing a context for high potential speciation rates. Conversely, ‘mature’ insular radiations exist with extensive co-occurrence of constituent taxa and substantial ecomorphological differentiation, which often confounded traditional taxonomy [ 7 , 12 – 15 ]. The rate of attaining reproductive isolation and the build-up of sympatry (i.e. assembly) on islands is understudied in non-adaptive radiations (e.g. away from Hawaii and the Galápagos; [ 16 – 18 ]). A key component is the critical stage after initial geographical expansion and subsequent diversification (i.e. allopatric speciation) when diversifying lineages initiate secondary sympatry among recently diverged populations. Unfortunately, most avian radiations are not suitable for studying the process of secondary sympatry on islands. For example, mature insular radiations provide only an incomplete picture because extinction, changes in distribution and substantial anagenesis obscures early stages of lineage accumulation, whereas purely geographical radiations (e.g. [ 10 ]) have not yet begun the process; thus, they are uninformative in the study of insular species assembly and secondary sympatry. Evidence from mature continental radiations supports a scenario of substantial divergence in allopatry before lineages are able, or have the opportunity, to co-occur [ 19 , 20 ]; however, factors that influence rates to secondary sympatry in continental systems are numerous: complex geography, closed ecological communities, disease transmission, biotic and abiotic environmental interactions, ecological similarity of sister taxa and complex signalling environments [ 20 – 25 ]. Conversely, insular systems are comparatively simple and may provide the most accessible insight into the tempo and mode of attaining secondary sympatry, even though extrapolation to diverse continental systems is difficult [ 17 ]. Here, we examine the phylogeographic and temporal patterns of diversification in the Todiramphus chloris species complex (Aves: Alcedinidae) and its close relatives. This species complex is the most widespread of the archetypal ‘great speciators’ [ 26 ], and comprises 50 nominal subspecies spanning a distance more than 16 000 km from the Red Sea to Samoa [ 27 – 29 ]. The full geographical extent of the genus extends a further 3000 km east to the Marquesas Islands in Eastern Polynesia (kingfishers do not occur in Hawaii). Most nominal subspecies correspond to single-island populations that are phenotypically distinct in plumage and size, but some islands/archipelagos have multiple sympatric Todiramphus species, including Palau, Vanuatu, and several islands in the Solomon Islands and the Bismarck Archipelago, as well as Australia. These instances of sympatry are presumed to be secondary (i.e. after allopatric speciation). Additionally, the distribution of Todiramphus sanctus —the only migratory Todiramphus —broadly overlaps many congeners in the T. chloris complex. All sympatric Todiramphus exhibit ecological, morphological and behavioural differences, including separation by habitat preference, suggesting a high degree of reproductive isolation between each pair [ 27 , 28 , 30 ]. Previous phylogenetic work on higher level kingfisher relationships showed extremely low genetic differentiation among five Todiramphus species [ 31 ], but only one T. chloris sample was included. With regard to non-adaptive (e.g. geographical) insular radiations, the T. chloris complex has several notable features. The broad distribution, numerous instances of closely related, sympatric species and close relationship between migratory and sedentary species make the T. chloris complex an ideal lineage for examining the consequence of rapid diversification and subsequent assembly of secondarily sympatric species in an insular system. 3. Material and methods 3.1 Taxon sampling Our 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 samples, 93 were T. chloris and 62 were composed of 15 additional Todiramphus species. We lacked only six Todiramphus species ( T. diops , T. lazuli , T. albonotatus , T. funebris , T. enigma and T. australasia ), owing to their distribution in areas where collecting fresh genetic source material is difficult. Our T. chloris sampling included 22 of 50 nominal subspecies [ 29 ]. Moyle [ 31 ] showed that Todiramphus is a clade distinct from Halcyon and sister to Syma ; therefore, we used Actenoides hombroni , Syma megarhyncha and Syma torotoro as outgroups to root trees. Whenever possible, we sequenced multiple individuals per population (i.e. per island) to guard against errors of misidentification, mislabelling or sample contamination. Figure 1. Map illustrating sampling of the Todiramphus chloris species complex used in this study. Circles, squares and triangles represent sampling points for T. chloris , T. sanctus and other (non- T. chloris ) ingroup taxa, respectively. Coloured distributions correspond to the 11 major phylogenetic lineages of the T. chloris species complex and match the coloured clades in the inset phylogeny. The inset topology is from the BEAST tree ( figure 3 ) with clades labelled A–G matching those from the M r B ayes tree ( figure 2 ). Points are not scaled to the number of sampled individuals per locality (the reader is referred to the electronic supplementary material, table S1 for numbers of individuals sampled). 3.2 DNA sequencing, alignment and model selection We extracted genomic DNA from frozen or alcohol-preserved muscle tissue, toepads of museum study skins or unvouchered blood samples (electronic supplementary material, table S1) using a non-commercial guanidine thiocyanate method [ 32 ]. For toepad extractions, we used laboratory space separate from other Todiramphus pre- and post-PCR products to minimize contamination risk [ 33 ]. We used unvouchered blood samples for taxa from remote islands in French Polynesia where collection of vouchered specimen material was not possible owing to small population sizes of endangered species (e.g. Todiramphus gambieri ; electronic supplementary material, table S1; [ 34 ]). We sequenced the entire second and third subunits of mitochondrial nicotinamide adenine dinucleotide dehydrogenase (hereafter ND2 and ND3, respectively) and four nuclear gene regions: the coiled-coil domain containing protein 132 (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 β 2 (TGF β 2) following protocols described in [ 35 ]. We used the following external primers in PCR amplification and sequencing: L5215 (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 modified external primers for CCDC132 and HMGB2 to better suit Todiramphus, and we designed internal primers to amplify 200–250 bp fragments of toepad samples (electronic supplementary material, table S2). We assembled and aligned sequence contigs in G eneious v. 6.1 (Biomatters), constructed individual nuclear intron alignments by hand, and checked them against an automated alignment in MUSCLE [ 42 ]. We phased introns in D na SP [ 43 ] with output threshold of 0.7 using algorithms provided by PHASE [ 44 , 45 ]. We identified appropriate models of sequence evolution for each of the seven partitions (electronic supplementary material, table S3) using Akaike's information criterion (AIC), as implemented in M r M odel T est v. 2.3 [ 46 ]. 3.3 Phylogenetic analysis We performed phylogenetic reconstruction on the total concatenated data, on separate concatenated mitochondrial DNA (mtDNA) and nuclear DNA (nDNA), and separately on each locus. We performed maximum-likelihood (ML) heuristic tree searches in GARLI v. 2.0 [ 47 ] and Bayesian analysis (BA) in M r B ayes v. 3.2.1 [ 48 – 50 ], implemented with BEAGLE [ 51 ]. We partitioned all ML and BA analyses by codon position for mtDNA and by gene for the nuclear introns. To avoid local optima in GARLI, we did 250 independent searches, each starting from a random tree. We adjusted GARLI's default parameters to terminate searches when no topological improvements were found after 100 000 generations (genthreshfortopoterm=100 000); otherwise, we used default settings. We assessed statistical support for the ML topology with 1000 non-parametric bootstrap replicates [ 52 ] and generated a 50% majority-rule consensus tree in S um T rees v. 3.3.1, part of the D endro P y v. 3.12.0 package [ 53 ]. In M r B ayes , we did four independent Markov chain Monte Carlo (MCMC) runs of 25 million generations using four chains per run (nchains=4) with incremental heating of chains (temp=0.1) sampled every 2500 generations. We changed the default branch length prior to unconstrained with an exponential distribution for all partitioned analyses to avoid artificially long branches (prset applyto=( all ) brlenspr=unconstrained:exponential(100); [ 54 ]). We assessed convergence of parameter estimates and tree splits in T racer v. 1.5 [ 55 ] and A re W e T here Y et ? (AWTY?; [ 56 , 57 ]), respectively. We assessed topology convergence between runs by the average standard deviation of split frequencies (ASDSF) and potential scale reduction factor. We discarded an appropriate number of burn-in generations based on convergence assessments of the ASDSF passing below 0.01; the remaining trees were summarized in a 50% majority-rule consensus tree. 3.4 Molecular dating and species delimitation We estimated divergence time in BEAST v. 1.7.5 [ 58 , 59 ] implemented with BEAGLE [ 51 ]. We included two individuals per nominal subspecies for all Todiramphus taxa, except T. sanctus , for which we included only known breeding populations (e.g. Australia, New Zealand, New Caledonia, Solomon Islands, Vanuatu and the Santa Cruz group; electronic supplementary material, table S1). We linked clock and tree models, but nucleotide substitution models were unlinked. We used M r M odel T est to partition the data in the same way we did our M r B ayes analyses (electronic supplementary material, table S3). We used a birth–death speciation process for the tree prior. To test for clock-like evolution, we compared 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 =1.0). Additionally, the coefficient of variation frequency histogram of the ucld.std parameter abutted against zero when viewed in T racer , which is a symptom that the data cannot reject a strict molecular clock [ 60 ]. We ran 10 independent MCMC chains for 100 million generations and sampled every 20 000th generation. We examined burn-in and convergence diagnostics in T racer ; burn-in values were specific to each run with at least 25% of samples discarded, with some runs requiring up to 40% burn-in. Lacking fossil calibration data for this group, we relied on published rates of mtDNA sequence evolution to calibrate our divergence dating analyses. Substitution rate priors derived from ND2 substitution rates for Hawaiian honeycreepers were used (0.024 and 0.033 substitutions per site Myr −1 ; [ 61 ]). We chose ND2 because it is one of the fastest-evolving mitochondrial gene regions in birds [ 61 ] and it is used widely among avian systematists and phylogeographers. We used a lognormal prior distribution for the clock.rate parameter with mean=0.029 and standard deviation=0.25. Using a general substitution rate from distantly related species is not ideal (e.g. kingfishers versus honeycreepers), but we note that mtDNA substitution rates across birds cluster around this value [ 19 , 62 ]. Regardless, these date estimates can only be used as a rough guide to clade ages. We used separate normally distributed substitution rate calibration priors for the three ND2 codon positions, whereas the introns were scaled to the mtDNA rate priors. ND3 was omitted from BEAST analyses to simplify mitochondrial rate calibrations. We examined species delimitation and diversification rates to objectively compare patterns of diversity in T. chloris to other published phylogenies of rapid geographical radiations (e.g. Zosterops and Erythropitta ). We delimited species with a Bayesian implementation of the general mixed Yule-coalescent model implemented in the R package, bGMYC [ 63 ]. We used the ND2 data and followed the authors' parameter 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 majority of phylogenetic signal occurs in the mtDNA, including rapid radiations like Todiramphus . We calculated diversification rates assuming a Yule process from the following formula: [ln( N )–ln( N o )]/ T , which uses initial diversity ( N o =2), extant diversity ( N ) and time ( T ) since origin of the crown clade [ 65 ]. 4. Results 4.1 Phylogenetic relationships Topologies inferred from multiple independent ML and BA runs were highly concordant. MCMC chain stationarity was achieved in M r B ayes (i.e. the ASDSF remained less than 0.01) after 8.15 million generations. Individual nuclear gene trees were largely uninformative at this shallow scale, but both mtDNA genes (ND2 and ND3) provided good phylogenetic resolution. No conflicting topologies were strongly supported between individual gene tree analyses (results not shown). The ingroup included all T. chloris samples plus 10 additional Todiramphus species ( figure 2 , clade A: posterior probability (PP) =1.0, bootstrap support (BS) =100). We defined this focal clade inclusive of T. farquhari because this circumscribed a suite of 11 closely related species subtended by a long internode that separated them from all other Todiramphus taxa. Multiple instances of sympatry exist within the focal clade, 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 ). Figure 2. Molecular phylogeny of the Todiramphus chloris species complex. The tree is the Bayesian maximum consensus tree from the concatenated, partitioned analysis with full sampling ( n =158 tips). Node support is denoted as Bayesian posterior probabilities/maximum-likelihood bootstrap support. Branch lengths of Actenoides and Syma were reduced to save space. Lettered clades (A–I) are discussed in the text. Clade A contained seven subclades ( figure 2 , clades B–I), each with PP=1.0, except clade F (PP=0.96), which includes T. cinnamominus from Guam and Pohnpei, and T. recurvirostris from Samoa. Of the 10 non- T. chloris species in the focal clade, clade C comprised five species endemic to Eastern Polynesia: T. godeffroyi , T. ruficollaris , T. veneratus , T. gambieri and T. tutus . Clade D was sister to clade C 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 Santa Cruz group. The placement of clades E and F was equivocal. The three subspecies of T. cinnamominus were split between these clades, rendering the species paraphyletic. The Palau endemic, T. c. pelewensis , was the sole member of clade E, whereas T. c. cinnamominus and T. c. reichenbachii , island endemics of Guam and Pohnpei, respectively, were sequentially sister to T. recurvirostris , itself an endemic of American Samoa. Clade G comprised T. chloris lineages from Australia and Papua New Guinea plus T. sanctus , which was embedded inside this clade. Clade H comprised three genetically distinct lineages: nominal T. c. chloris from Sulawesi, T. c. humii from Singapore, and a clade that comprised multiple subspecies from Borneo to the Philippines and Palau. Finally, clade I included lineages from such geographically disparate regions as Melanesia and the Mariana Islands. Todiramphus saurophagus was sister to T. c. albicilla + T. c. orii from Saipan and Rota, Mariana Islands. The other half of clade I included T. c. nusae and T. c. alberti of the Bismarck Archipelago and Solomon Islands, respectively, to the exclusion of the eastern Solomon Islands (Makira, Ugi and Rennell; clade D). 4.2 Divergence times, diversification rates and species limits Todiramphus diversified rapidly and recently. The ND2 sequence divergence within the focal clade (clade A) was 2.2% (median ND2 uncorrected P distance between T. farquhari and all remaining clade A taxa). The maximum pairwise divergence (3.4%) occurred between the Southeast Asian clade, including nominate T. c. chloris (clade H) and the eastern Polynesian clade (clade C). We used two rates of ND2 sequence divergence derived from the 95% CI range from Hawaiian honeycreeper mitogenomes (0.024 and 0.033 substitutions per site Myr −1 ; [ 61 ]) to calibrate the clock prior in our BEAST analysis. The faster rate (3.3%) results in a younger age estimate, whereas the slower rate results in an older estimate. These calibrations place the start of diversification of clade A in the mid-Pleistocene, approximately 0.57–0.85 Myr ago (mean 0.71 Ma; figure 3 ). We caution against strict interpretation of these values because divergence time estimation based on a molecular clock has numerous shortcomings, especially when based on single-gene calibrations from distantly related species, as well as in the absence of fossil or island-age calibrations. Figure 3. Time-calibrated maximum clade credibility tree with 95% highest posterior density bars from the BEAST analysis. Node support is given as Bayesian posterior probability (PP): black circles at nodes denote PP=1.0, grey circles denote 0.95≤PP≤0.99. Unlabelled nodes denote PP<0.95. The red vertical line denotes the bGMYC species delimitation estimate (i.e. the bGMYC analysis identified as species all clades to the right of the line). Sympatric lineages are identified by colour-coded labels that correspond to their respective distributions 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 (A–I) 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. juliae , respectively). Illustrations courtesy of the Handbook of the Birds of the World , Lynx Edicions. Threshold species delimitation with bGMYC suggested that current species diversity is vastly underestimated in Todiramphus . Current taxonomic authorities [ 29 ] recognize 11 biological species that are nested within our clade A. The bGMYC estimate, based on ND2 data only, found strong support for 26 species within clade A plus seven species outside it (i.e. outgroup taxa; figure 3 ). This estimate of 26 ingroup species probably is conservative because we lacked 28 of the 50 nominal subspecies of T. chloris . We calculated two pairs of diversification rates based on estimates of species diversity in clade A: the more conservative 11 ‘bio-species’ (e.g. following current taxonomy; [ 29 ]) and our more liberal bGMYC estimate of 26 ingroup species. For each ingroup species scenario (11 and 26 species, respectively), we calculated diversification rates based on the range of crown clade ages derived from the BEAST divergence time estimation (0.57–0.85 Myr ago). Thus, our conservative estimate ( n =11 ingroup species) yields a diversification rate of 2.01–2.99 sp Myr −1 , whereas our bGMYC-based estimate ( n =26 ingroup species) is 3.02–4.49 sp Myr −1 , 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 diversification rate estimate probably would be higher. 5. Discussion 5.1 Timing and rates of diversification Phylogenetic results indicate that characterization of T. chloris as a ‘great speciator’ [ 26 ] was not quite accurate, because T. chloris is not a natural group. Indeed, the reality is even more striking; 10 species were found to be embedded within or minimally divergent from T. chloris , rendering it paraphyletic. Unbeknownst to Diamond et al . [ 26 ] in their description of the paradox of the great speciators, rapid geographical diversification of the T. chloris complex was accompanied by several instances of secondary sympatry involving morphologically disparate taxa ( figure 3 ), which obscured their evolutionary relationships. Phylogenetic reconstruction and molecular dating estimates revealed that the T. chloris complex is extremely young and reached its geographical distribution quite rapidly. The divergence between T. farquhari and the rest of the ingroup was only 2.2% (ND2 uncorrected P), which yielded a crown clade divergence time estimate for the complex between 0.57 and 0.85 Ma. This time frame in the mid-Pleistocene is more recent than the diversification of the red-bellied pitta Erythropitta erythrogaster throughout the Philippines, Wallacea and New Guinea (approx. 1.8 Ma; [ 10 ]). However, we caution against drawing specific conclusions based on these time estimates because of myriad shortcomings of molecular clock calibrations for divergence time estimation [ 67 – 69 ]. Nevertheless, our estimates of divergence time and species-level diversity (i.e. unique evolutionary lineages) produced high diversification rate estimates compared with other birds [ 70 ]. Overall, we interpret the striking pattern of shallow internodes at the base and relatively shallow divergences between ingroup taxa as support for a scenario in which Todiramphus achieved its full geographical distribution—from French Polynesia to the Sunda Shelf (and possibly the Red Sea, although those populations were not sampled)—rapidly and recently. Similar patterns have been noted in other Pacific bird lineages, including Acrocephalus reed-warblers [ 71 ], Alopecoenas doves [ 72 , 73 ], Ceyx kingfishers [ 11 ], Erythropitta pittas [ 10 ], Pachycephala whistlers [ 35 , 74 ] and Zosterops white-eyes [ 66 ]. However, not all Pacific bird lineages fit this pattern of rapid and widespread diversification; monarch flycatchers [ 7 ] and Ptilinopus fruit-doves [ 75 ] are two examples of widespread, ‘mature’ lineages that have been diversifying throughout the Pacific for much longer. 5.2 Secondary sympatry, shifting dispersal ability and migration Reduction in dispersal ability or propensity after geographical expansion is a leading hypothesis for diversification of rapid geographical radiations in island settings [ 6 , 26 , 76 ]. Although rapid reduction of dispersal ability would allow for differentiation among island populations, it would seemingly prevent secondary colonization that is required to achieve sympatry. This key evolutionary juncture is where the paradox of the great speciators [ 26 ] and the taxon cycles hypothesis [ 6 ] intersect: together, these hypotheses allow for differentiation and build-up of secondary sympatry with repeated colonization. Among insular avian radiations, a clear dichotomy exists between lineages that underwent expansive geographical differentiation but rarely or never attained secondary sympatry [ 10 , 11 , 35 , 74 ], and those that display both broad geographical diversification as well as build-up of sympatric diversity [ 7 , 13 , 15 , 75 ]. This can be seen in the Ceyx lepidus species complex (Aves: Alcedinidae), which has geographical replacement populations across approximately 5000 km of the southwest Pacific, but has only attained sympatry with close relatives in portions of the Philippines [ 11 ]. Like Todiramphus, the phylogeny of C. lepidus has shallow internodes at the base with long branches subtending extant island populations. This pattern is consistent with rapid geographical expansion followed by reduction in dispersal ability across all of C. lepidus . Based on our molecular dates, C. lepidus is about twice as old as the entire T. chloris radiation. Clade age can affect interpretation of diversification rate [ 77 , 78 ], but it appears that C. lepidus is a lineage whose diversification slowed after an initial stage of rapid geographical expansion. Reduction in dispersal propensity, however, need not proceed uniformly across a clade. Indeed, rails, Ptilinopus fruit-doves and Zosterops white-eyes, show marked differences in dispersal ability among closely related lineages across the Pacific [ 66 , 75 , 79 – 81 ]. Importantly, all three groups also have substantial secondary sympatry among species (rails did prior to widespread extinction), which coincides with dispersive taxa. Wilson [ 82 ] noted the possibility of this uneven change in dispersal ability within a diversifying lineage in the context of cyclic expansion and contraction phases in diversification. The layering of Todiramphus taxa resulting from such cycles is best illustrated in the Solomon Islands. Four Todiramphus species breed on the larger islands and are clearly differentiated by age, habitat and inferred dispersal propensity ( figure 3 ). In the context of Diamond's [ 26 ] and Wilson's [ 6 ] views on the influence of variable dispersal abilities on diversification patterns, the T. chloris complex contains multiple instances of secondary sympatry that juxtapose taxa with markedly different dispersal histories. The incidence of secondary sympatry across the Pacific distribution of the T. chloris group is remarkably high given the recency of the radiation. In every case, the sympatric lineages diverged substantially in terms of phenotype, morphology, ecology, dispersal ability/propensity and/or behaviour. For example, Palau holds two Todiramphus species: T. cinnamominus pelewensis and T. chloris teraokai. These taxa have diverged morphologically and in habitat preference, such that T. c. pelewensis is ca . 50% smaller in body mass and inhabits forest interior, whereas T. chloris teraokai is larger and prefers coconut groves and beaches [ 30 , 83 ]. The species differ in plumage as well: T. c. pelewensis has an orange crown, whereas T. chloris teraokai has a blue-green crown typical of many T. chloris forms. A difference in dispersal history can be inferred from distributions and genetic structure of the two taxa: T. c. pelewensis is restricted to the Palau Archipelago and a relatively large genetic divergence separates it from its nearest relative. By contrast, T. chloris teraokai is embedded in a relatively undifferentiated clade that also spans the Philippine archipelago and Borneo. It appears that Palau was first colonized by T. cinnamominus , with T. chloris arriving quite recently ( figure 3 ). This nested pattern of old and young lineages within an archipelago was also noted recently in Ptilinopus fruit-doves from 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 saurophagus is the largest species in the genus; it is twice the size of the sympatric T. chloris forms, and it differs phenotypically from most other Todiramphus in having a completely white head (save a blue post-ocular stripe). It inhabits beaches, coastal forest, reefs, islets and occasionally mangroves, but never ventures far from the coast. Throughout its distribution from the northern Moluccas to the Solomon Islands, it is sympatric with one to two species of Todiramphus , including representative T. chloris forms. For example, T. chloris alberti and T. chloris nusae occur in the Solomon Islands and Bismarck Archipelago, respectively, where they inhabit secondary forest and open areas away from the coast. Notably, T. saurophagus and both T. chloris subspecies are in the same subclade of the T. chloris phylogeny and diverged from one another quite recently, perhaps 0.5 Ma ( figure 3 ). The most complex scenario of secondary sympatry in Todiramphus occurs in clade G ( figure 2 ). This clade comprises all T. chloris from Australia and New Guinea, which are split in two lineages: (i) an endemic to the Milne Bay Province islands of southeast Papua New Guinea, T. c. colonus ; and (ii) the Australian clade, T. c. sordidus + T. c. colcloughi . These allopatric lineages occur in different habitats: forest edge on small islands in the D'Entrecasteaux and Louisiade Archipelagos ( T. c. colonus ) and mangrove 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 populations are highly migratory. Its breeding range spans Australia, New Zealand, New Caledonia and parts of the Solomon Islands. Many populations migrate north in the austral winter to the Sunda Shelf, New Guinea and Northern Melanesia. We sampled three of the five nominal subspecies [ 29 ], including two from previously unknown localities (Nendo Island, Santa Cruz group and Espiritu Santo, Vanuatu), and despite the geographical complexity of this species' distribution, there was no genetic substructure within T. sanctus ; individuals from migratory and sedentary populations across their broad distribution are intermixed in the clade. Sympatric forms of T. chloris and T. sanctus differ ecomorphologically and behaviourally. Todiramphus sanctus is smaller than any sympatric T. chloris throughout its range. Behaviourally, the migratory nature of T. sanctus is novel in Todiramphus kingfishers. This behaviour is particularly relevant in light of the ‘great speciators’ paradox [ 26 ]. The paradox poses the question: why are some species geographically widespread, implying high dispersal ability, but at the same time well-differentiated across even narrow water gaps, implying low dispersal ability? Diamond et al . [ 26 ] suggested that some of the ‘great speciators’ underwent colonization cycles in which they had past phases of higher immigration rates and dispersal abilities followed by a loss of dispersal ability with subsequent differentiation on newfound islands. They count Todiramphus [ Halcyon ] chloris among the several lineages as evidence for this idea. That the migratory T. sanctus is so closely related to T. chloris —especially given its placement deeply embedded in the phylogeny—emphasizes the potential role of shifts in dispersal ability as a driver of diversification. It is possible that the migratory nature of T. sanctus is an evolutionary vestige of the ancestral Todiramphus lineage still exhibiting the colonization phase of Diamond et al . [ 26 ]. If so, T. sanctus offers intriguing evidence in support of this component of the paradox. Rapid reduction of dispersal ability in island birds has been suspected [ 66 , 84 , 85 ], and evidence suggests that morphological change is not necessary for such a shift in dispersal ability; it can be entirely behavioural [ 86 ]. It has also been shown that birds can acquire migratory ability quickly in response to selective pressure [ 87 , 88 ], and this trait is thought to be evolutionarily labile [ 89 ]. A prevailing paradigm is that extant migratory species evolved from sedentary tropical ancestors [ 90 ], however, recent evidence in emberizoid passerines suggests otherwise [ 91 , 92 ]. Loss of migration may be as common as gains and extant sedentary tropical radiations (e.g. some Geothlypis and a clade containing Myiothlypis , Basileuterus and Myioborus ) represent at least two losses of latitudinal migration with possible colonization of the tropics from the temperate region [ 91 ]. 6. Conclusion Early biogeographers such as Darwin, Wallace and Darlington appreciated that lineages can diversify across vast insular systems. Subsequent observation led to description of similar patterns across many of these radiations and formulation of hypotheses to explain them (e.g. ‘Taxon Cycles’ and ‘Great Speciators’). We showed that the T. chloris group exhibits three characteristics of particular interest in discussions of how diversity accumulates on islands. First, the group diversified rapidly concomitant with a geographical expansion covering approximately 16 000 km of longitude. This diversification rate is among the most rapid known in birds [ 66 , 70 ]. Second, within the short time frame of diversification, secondary sympatry has been achieved multiple times. Although it is unmeasured 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, extreme disparity in dispersal ability has evolved within the group—migratory T. sanctus is embedded within the sedentary T. chloris complex. Together, these aspects support a hypothesis that rapid and uneven shifts in dispersal propensity across clades have been prominent in moulding the evolution of insular biotas. Supplementary Material Appendix: Biogeography and species limits; Tables 1-3. Acknowledgements We are grateful to the following collections managers and curators for providing loans of tissue or toepad samples from their institutions: Paul Sweet, Peter Capainolo, Tom Trombone and Joel Cracraft, American Museum of Natural History; Robert Palmer and Leo Joseph, Australian National Wildlife Collection; Andrew Kratter and David Steadman, University of Florida Museum of Natural History; Donna Dittmann, Louisiana State University Museum of Natural Science; Mark Robbins, University of Kansas Biodiversity Institute; Eric Pasquet, Muséum National d'Histoire Naturelle, Paris; Rob Fleischer, Smithsonian National Zoological Park; Sharon Birks, University of Washington Burke Museum. M.J.A. and R.G.M. thank Alivereti Naikatini, Marika Tuiwawa, Mika Bolakania, Sanivalati Vido, Lulu Cakacaka and Joeli Vakabua for assistance with permits and fieldwork in Fiji; the Department of Environment and Conservation, NRI (Georgia Kaipu) and PNGIBR (Miriam Supuma) for assistance and permission to work in Papua New Guinea; the Ministry of Environment, Climate Change, Disaster Management and Meterology in Solomon Islands; Protected Areas and Wildlife Bureau of the Philippine Department of Environment and Natural Resources; CNMI Division of Fish & Wildlife (Paul Radley) in the Mariana Islands; and Belau National Museum (Allan Olsen), Division of Fish and Wildlife Protection (Kammen Chin), Bureau of Agriculture (Fred Sengebau, Gwen Bai and Hilda Etpison), and the Koror State Office (Hulda Blesam) in Palau. A.C. and J.-C.T. thank Jean-Yves Meyer (Research delegation of the Government of French Polynesia), Philippe Raust (Société d'Ornithologie de Polynésie), Claude Serra (Direction de l'Environnement, French Polynesia), and the Institut pour la Recherche et le Développement (IRD Tahiti) for their help and support during fieldwork in French Polynesia. We are grateful to Lynx Edicions for permission to use illustrations from the Handbook of the Birds of the World series (illustrated by Norman Arlott). Helpful comments were provided by Brian T. Smith, H. Douglas Pratt, Thane Pratt, Matthew L. Knope and one anonymous reviewer. Ethics statement This project operated under IACUC approval AUS no. 174-01, issued to R.G.M. at the University of Kansas. Data accessibility All DNA sequences generated in this study are deposited in GenBank under accession numbers ( KP291162–KP292029 ). Authors contributions M.J.A. and R.G.M. conceived the design of this project. M.J.A., A.C., J.-C.T., C.E.F. and R.G.M. conducted fieldwork. M.J.A., H.T.S. and A.C. carried out the molecular laboratory work and sequence alignments. M.J.A. conducted the data analysis and drafted the manuscript, together with R.G.M. All authors participated in editing the manuscript, and all authors gave final approval for publication. Funding statement This project was funded in part by an American Museum of Natural History Chapman Fellowship (M.J.A.), an American Ornithologists' Union Research Award (M.J.A.), a University of Kansas Doctoral Student Research Fund (M.J.A.) and NSF DEB-1241181 and DEB-0743491 (R.G.M.). Competing interests The authors claim no competing interests in this work. References 1 Mayr E 1942 Systematics and the origin of species. New York, NY : Columbia University Press . 2 Mayr E , Diamond J 2001 The birds of Northern Melanesia: speciation, ecology, and biogeography. New York, NY : Oxford University Press . 3 Diamond JM 1977 Continental and insular speciation in Pacific land birds. Syst. Zool. 26 , 263 – 268 . ( doi:10.2307/2412673 ) 4 Lack D 1947 Darwin's finches. Cambridge, UK : Cambridge University Press . 5 MacArthur RH , Wilson EO 1967 The theory of island biogeography. Princeton, NJ : Princeton University Press . 6 Wilson EO 1961 The nature of the taxon cycle in the Melanesian ant fauna. Am. Nat. 95 , 169 – 193 . ( doi:10.1086/282174 ) 7 Filardi CE , Moyle RG 2005 Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature 438 , 216 – 219 . ( doi:10.1038/nature04057 ) 16281034 10.1038/nature04057 8 Dávalos LM 2007 Short-faced bats (Phyllostomidae: Stenodermatina): a Caribbean radiation of strict frugivores. J. Biogeogr. 34 , 364 – 375 . ( doi:10.1111/j.1365-2699.2006.01610.x ) 9 Hutsemékers V , Szövényi P , Shaw AJ , González-Mancebo J-M , Muñoz J , Vanderpoorten A 2011 Oceanic islands are not sinks of biodiversity in spore-producing plants. Proc. Natl Acad. Sci. USA 108 , 18989 – 18994 . ( doi:10.1073/pnas.1109119108 ) 22084108 10.1073/pnas.1109119108 PMC3223459 10 Irestedt M , Fabre P-H , Batalha-Filho H , Jønsson KA , Roselaar CS , Sangster G , Ericson PGP The spatio-temporal colonization and diversification across the Indo-Pacific by a ‘great speciator’ (Aves, Erythropitta erythrogaster) . Proc. R. Soc. B 2013 280 , 20130309 ( doi:10.1098/rspb.2013.0309 ) 10.1098/rspb.2013.0309 PMC3619518 23554394 11 Andersen MJ , Oliveros CH , Filardi CE , Moyle RG 2013 Phylogeography of the variable dwarf-kingfisher Ceyx lepidus (Aves: Alcedinidae) inferred from mitochondrial and nuclear DNA sequences. Auk 130 , 118 – 131 . ( doi:10.1525/auk.2012.12102 ) 12 Uy JAC , Moyle RG , Filardi CE 2009 Plumage and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands. Evolution 63 , 153 – 164 . ( doi:10.1111/j.1558-5646.2008.00530.x ) 18803681 10.1111/j.1558-5646.2008.00530.x 13 Nyári ÁS , Benz BW , Jønsson KA , Fjeldså J , Moyle RG 2009 Phylogenetic relationships of fantails (Aves: Rhipiduridae). Zool. Scr. 38 , 553 – 561 . ( doi:10.1111/j.1463-6409.2009.00397.x ) 14 Andersen MJ , Naikatini A , Moyle RG 2014 A molecular phylogeny of Pacific honeyeaters (Aves: Meliphagidae) reveals extensive paraphyly and an isolated Polynesian radiation. Mol. Phylogenet. Evol. 71 , 308 – 315 . ( doi:10.1016/j.ympev.2013.11.014 ) 24315868 10.1016/j.ympev.2013.11.014 15 Jønsson KA , Bowie RCK , Nylander JAA , Christidis L , Norman JA , Fjeldså J 2010 Biogeographical history of cuckoo-shrikes (Aves: Passeriformes): transoceanic colonization of Africa from Australo-Papua. J. Biogeogr. 37 , 1767 – 1781 . ( doi:10.1111/j.1365-2699.2010.02328.x ) 16 Gillespie R 2004 Community assembly through adaptive radiation in Hawaiian spiders. Science 303 , 356 – 359 . ( doi:10.1126/science.1091875 ) 14726588 10.1126/science.1091875 17 Losos JB , Ricklefs RE 2009 Adaptation and diversification on islands. Nature 457 , 830 – 836 . ( doi:10.1038/nature07893 ) 19212401 10.1038/nature07893 18 Weeks BC , Claramunt S 2014 Dispersal has inhibited avian diversification in Australasian archipelagoes. Proc. R. Soc. B 281 , 20141257 ( doi:10.1098/rspb.2014.1257 ) 10.1098/rspb.2014.1257 PMC4132686 25100701 19 Weir JT , Price TD 2011 Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177 , 462 – 469 . ( doi:10.1086/658910 ) 21460568 10.1086/658910 20 Tobias JA , Cornwallis CK , Derryberry EP , Claramunt S , Brumfield RT , Seddon N 2013 Species coexistence and the dynamics of phenotypic evolution in adaptive radiation. Nature 506 , 359 – 363 . ( doi:10.1038/nature12874 ) 24362572 10.1038/nature12874 21 Ricklefs RE 2010 Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space. Proc. Natl Acad. Sci. USA 107 , 1265 – 1272 . ( doi:10.1073/pnas.0913626107 ) 20080597 10.1073/pnas.0913626107 PMC2824412 22 Ricklefs RE 2010 Host–pathogen coevolution, secondary sympatry and species diversification. Phil. Trans. R. Soc. B 365 , 1139 – 1147 . ( doi:10.1098/rstb.2009.0279 ) 20194175 10.1098/rstb.2009.0279 PMC2830228 23 Peterson AT , Soberón J , Sánchez-Cordero V 1999 Conservatism of ecological niches in evolutionary time. Science 285 , 1265 – 1267 . ( doi:10.1126/science.285.5431.1265 ) 10455053 10.1126/science.285.5431.1265 24 Pigot AL , Tobias JA 2013 Species interactions constrain geographic range expansion over evolutionary time. Ecol. Lett. 16 , 330 – 338 . ( doi:10.1111/ele.12043 ) 23231353 10.1111/ele.12043 25 Tobias JA , Planqué R , Cram DL , Seddon N 2014 Species interactions and the structure of complex communication networks. Proc. Natl Acad. Sci. USA 111 , 1020 – 1025 . ( doi:10.1073/pnas.1314337111 ) 24395769 10.1073/pnas.1314337111 PMC3903186 26 Diamond JM , Gilpin ME , Mayr E 1976 Species-distance relation for birds of the Solomon Archipelago, and the paradox of the great speciators. Proc. Natl Acad. Sci. USA 73 , 2160 – 2164 . ( doi:10.1073/pnas.73.6.2160 ) 16592328 10.1073/pnas.73.6.2160 PMC430470 27 Fry CH , Fry K , Harris A 1992 Kingfishers, bee-eaters & rollers: a handbook 324 p. Princeton, NJ : Princeton University Press . 28 Woodall PF 2001 Family Alcedinidae (kingfishers) . In Handbook of the Birds of the World . vol. 6 Mousebirds to hornbills (eds del Hoyo J , Elliott A and Sargatal J ), pp. 130 – 249 . Barcelona, Spain : Lynx Edicions . 29 Gill FB , Donsker D 2014 IOC World Bird List (v.4.3). See http://www.worldbirdnames.org 30 Fry CH 1980 The evolutionary biology of kingfishers (Alcedinidae). Living Bird. 18 , 113 – 160 . 31 Moyle RG 2006 A molecular phylogeny of kingfishers (Alcedinidae) with insights into early biogeographic history. Auk 123 , 487 – 499 . ( doi:10.1642/0004-8038(2006)123[487:AMPOKA]2.0.CO;2 ) 32 Esselstyn JA , Garcia HJD , Saulog MG , Heaney LR 2008 A new species of Desmalopex (Pteropodidae) from the Philippines, with a phylogenetic analysis of the Pteropodini. J. Mammal. 89 , 815 – 825 . ( doi:10.1644/07-MAMM-A-285.1 ) 33 Mundy NI , Unitt P , Woodruff DS 1997 Skin from feet of museum specimens as a non-destructive source of DNA for avian genotyping. Auk 114 , 126 – 129 . ( doi:10.2307/4089075 ) 34 Kesler DC , Haig SM 2007 Conservation biology for suites of species: demographic modeling for Pacific island kingfishers. Biol. Conserv. 136 , 520 – 530 . ( doi:10.1016/j.biocon.2006.12.023 ) 35 Andersen MJ , Nyári ÁS , Mason I , Joseph L , Dumbacher JP , Filardi CE , Moyle RG 2014 Molecular systematics of the world's most polytypic bird: the Pachycephala pectoralis/melanura (Aves: Pachycephalidae) species complex. Zool. J. Linn. Soc. 170 , 566 – 588 . ( doi:10.1111/zoj.12088 ) 36 Hackett SJ 1996 Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Mol. Phylogenet. Evol. 5 , 368 – 382 . ( doi:10.1006/mpev.1996.0032 ) 8728395 10.1006/mpev.1996.0032 37 Johnson KP , Sorenson MD 1998 Comparing molecular evolution in two mitochondrial protein coding genes (cytochrome $b$ and ND2) in the dabbling ducks (Tribe: Anatini). Mol. Phylogenet. Evol. 10 , 82 – 94 . ( doi:10.1006/mpev.1997.0481 ) 9751919 10.1006/mpev.1997.0481 38 Chesser RT 1999 Molecular systematics of the rhinocryptid genus Pteroptochos. Condor 101 , 439 – 446 . ( doi:10.2307/1370012 ) 39 Backström N , Fagerberg S , Ellegren H 2008 Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol. Ecol. 17 , 964 – 980 . ( doi:10.1111/j.1365-294X.2007.03551.x ) 17927703 10.1111/j.1365-294X.2007.03551.x 40 Kimball RT et al 2009 A well-tested set of primers to amplify regions spread across the avian genome. Mol. Phylogenet. Evol. 50 , 654 – 660 . ( doi:10.1016/j.ympev.2008.11.018 ) 19084073 10.1016/j.ympev.2008.11.018 41 Primmer CR , Borge T , Lindell J , Sætre GP 2002 Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol. Ecol. 11 , 603 – 612 . ( doi:10.1046/j.0962-1083.2001.01452.x ) 11918793 10.1046/j.0962-1083.2001.01452.x 42 Edgar RC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 , 1792 – 1797 . ( doi:10.1093/nar/gkh340 ) 15034147 10.1093/nar/gkh340 PMC390337 43 Librado P , Rozas J 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 , 1451 – 1452 . ( doi:10.1093/bioinformatics/btp187 ) 19346325 10.1093/bioinformatics/btp187 44 Stephens M , Donnelly P 2003 A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73 , 1162 – 1169 . ( doi:10.1086/379378 ) 14574645 10.1086/379378 PMC1180495 45 Stephens M , Smith NJ , Donnelly P 2001 A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68 , 978 – 989 . ( doi:10.1086/319501 ) 11254454 10.1086/319501 PMC1275651 46 Nylander JAA 2004 MrModelTest v2. (Program distributed by the author. Evolutionary Biology Centre, Uppsala University 47 Zwickl DJ 2006 Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Austin, TX : The University of Texas . 48 Ronquist F , Huelsenbeck JP 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 , 1572 – 1574 . ( doi:10.1093/bioinformatics/btg180 ) 12912839 10.1093/bioinformatics/btg180 49 Altekar G , Dwarkadas S , Huelsenbeck JP , Ronquist F 2004 Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20 , 407 – 415 . ( doi:10.1093/bioinformatics/btg427 ) 14960467 10.1093/bioinformatics/btg427 50 Ronquist F et al 2012 M r B ayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space . 61 , 539 – 542 . ( doi:10.1093/sysbio/sys029 ) 10.1093/sysbio/sys029 PMC3329765 22357727 51 Ayres DL et al 2012 BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Syst. Biol. 61 , 170 – 173 . ( doi:10.1093/sysbio/syr100 ) 21963610 10.1093/sysbio/syr100 PMC3243739 52 Felsenstein J 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 , 783 – 791 . ( doi:10.2307/2408678 ) 10.1111/j.1558-5646.1985.tb00420.x 28561359 53 Sukumaran J , Holder MT 2010 DendroPy: a Python library for phylogenetic computing. Bioinformatics 26 , 1569 – 1571 . ( doi:10.1093/bioinformatics/btq228 ) 20421198 10.1093/bioinformatics/btq228 54 Brown JM , Hedtke SM , Lemmon AR , Lemmon EM 2010 When trees grow too long: investigating the causes of highly inaccurate Bayesian branch-length estimates. Syst. Biol. 59 , 145 – 161 . ( doi:10.1093/sysbio/syp081 ) 20525627 10.1093/sysbio/syp081 55 Rambaut A , Drummond A 2007 Tracer v.1.5. See http://tree.bio.ed.ac.uk/software/tracer/ 56 Nylander JAA , Wilgenbusch JC , Warren DL , Swofford DL 2008 AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24 , 581 – 583 . ( doi:10.1093/bioinformatics/btm388 ) 17766271 10.1093/bioinformatics/btm388 57 Wilgenbusch JC , Warren DL , Swofford DL 2004 AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. See http://ceb.csit.fsu.edu/awty/ 10.1093/bioinformatics/btm388 17766271 58 Drummond AJ , Suchard MA , Xie D , Rambaut A 2012 Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29 , 1969 – 1973 . ( doi:10.1093/molbev/mss075 ) 22367748 10.1093/molbev/mss075 PMC3408070 59 Drummond AJ , Nicholls GK , Rodrigo AG , Solomon W 2002 Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161 , 1307 – 1320 . 12136032 10.1093/genetics/161.3.1307 PMC1462188 60 Drummond AJ , Ho SYW , Rawlence N , Rambaut A 2007 A rough guide to BEAST 1.4 (retrieved 1 April 2014). See http://workshop.molecularevolution.org/molevolfiles/beast/BEAST14_MANUAL-7-6-07.pdf 61 Lerner HR , Meyer M , James HF , Hofreiter M , Fleischer RC 2011 Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr. Biol. 21 , 1838 – 1844 . ( doi:10.1016/j.cub.2011.09.039 ) 22018543 10.1016/j.cub.2011.09.039 62 Weir JT , Bermingham E , Miller MJ , Klicka J , Gonzalez MA 2008 Phylogeography of a morphologically diverse Neotropical montane species, the common bush-tanager (Chlorospingus ophthalmicus). Mol. Phyl. Evol. 47 , 650 – 664 . ( doi:10.1016/j.ympev.2008.02.004 ) 10.1016/j.ympev.2008.02.004 18378470 63 Reid NM , Carstens BC 2012 Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol. Biol. 12 , 196 ( doi:10.1186/1471-2148-12-196 ) 23031350 10.1186/1471-2148-12-196 PMC3503838 64 Pons J , Barraclough T , Gomez-Zurita J , Cardoso A , Duran D , Hazell S , Kamoun S , Sumlin W , Vogler A 2006 Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55 , 595 – 609 . ( doi:10.1080/10635150600852011 ) 16967577 10.1080/10635150600852011 65 Magallon S , Sanderson MJ 2001 Absolute diversification rates in angiosperm clades. Evolution 55 , 1762 – 1780 . ( doi:10.1111/j.0014-3820.2001.tb00826.x ) 11681732 10.1111/j.0014-3820.2001.tb00826.x 66 Moyle RG , Filardi CE , Smith CE , Diamond JM 2009 Explosive Pleistocene diversification and hemispheric expansion of a great speciator. Proc. Natl Acad. Sci. USA 106 , 1863 – 1868 . ( doi:10.1073/pnas.0809861105 ) 19181851 10.1073/pnas.0809861105 PMC2644129 67 Lovette IJ 2004 Mitochondrial dating and mixed support for the ‘2%’ rule in birds . Auk 121 , 1 – 16 . 68 Arbogast BS , Edwards SV , Wakeley J , Beerli P , Slowinski JB 2002 Estimating divergence times from molecular data on phylogenetic and population genetics timescales. Annu. Rev. Ecol. Syst. 33 , 707 – 740 . ( doi:10.1146/annurev.ecolsys.33.010802.150500 ) 69 Lanfear R , Welch JJ , Bromham L 2010 Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol. Evol. 25 , 495 – 503 . ( doi:10.1016/j.tree.2010.06.007 ) 20655615 10.1016/j.tree.2010.06.007 70 Jetz W , Thomas GH , Joy JB , Hartmann K , Mooers AO 2012 The global diversity of birds in space and time. Nature 491 , 444 – 448 . ( doi:10.1038/nature11631 ) 23123857 10.1038/nature11631 71 Cibois A , Beadell JS , Graves GR , Pasquet E , Slikas B , Sonsthagen SA , Thibault J-C , Fleischer RC 2011 Charting the course of reed-warblers across the Pacific islands. J. Biogeogr. 38 , 1963 – 1975 . ( doi:10.1111/j.1365-2699.2011.02542.x ) 72 Moyle RG , Jones RM , Andersen MJ 2013 A reconsideration of Gallicolumba (Aves: Columbidae) relationships using fresh source material reveals pseudogenes, chimeras, and a novel phylogenetic hypothesis. Mol. Phylogenet. Evol. 66 , 1060 – 1066 . ( doi:10.1016/j.ympev.2012.11.024 ) 23220516 10.1016/j.ympev.2012.11.024 73 Jønsson KA , Irestedt M , Bowie RCK , Christidis L , Fjeldså J 2011 Systematics and biogeography of Indo-Pacific ground-doves. Mol. Phylogenet. Evol. 59 , 538 – 543 . ( doi:10.1016/j.ympev.2011.01.007 ) 21256968 10.1016/j.ympev.2011.01.007 74 Jønsson KA , Irestedt M , Christidis L , Clegg SM , Holt BG , Fjeldsa J 2014 Evidence of taxon cycles in an Indo-Pacific passerine bird radiation (Aves: Pachycephala). Proc. R. Soc. B 281 , 20131727 ( doi:10.1098/rspb.2013.1727 ) 10.1098/rspb.2013.1727 PMC3896003 24403319 75 Cibois A , Thibault J-C , Bonillo C , Filardi CE , Watling D , Pasquet E 2014 Phylogeny and biogeography of the fruit doves (Aves: Columbidae). Mol. Phylogenet. Evol. 70 , 442 – 453 . ( doi:10.1016/j.ympev.2013.08.019 ) 24012584 10.1016/j.ympev.2013.08.019 76 Carlquist SJ 1974 Island biology ix, 660 pp New York, NY : Columbia University Press . 77 Knope ML , Morden CW , Funk VA , Fukami T 2012 Area and the rapid radiation of Hawaiian Bidens (Asteraceae). J. Biogeogr. 39 , 1206 – 1216 . ( doi:10.1111/j.1365-2699.2012.02687.x ) 78 Rabosky DL 2009 Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecol. Lett. 12 , 735 – 743 . ( doi:10.1111/j.1461-0248.2009.01333.x ) 19558515 10.1111/j.1461-0248.2009.01333.x 79 Bertrand JAM et al 2014 Extremely reduced dispersal and gene flow in an island bird. Heredity 112 , 190 – 196 . ( doi:10.1038/hdy.2013.91 ) 24084644 10.1038/hdy.2013.91 PMC3907105 80 Slikas B , Olson SL , Fleischer RC 2002 Rapid, independent evolution of flightlessness in four species of Pacific Island rails (Rallidae): an analysis based on mitochondrial sequence data. J. Avian. Biol. 33 , 5 – 14 . ( doi:10.1034/j.1600-048X.2002.330103.x ) 81 Kirchman JJ 2012 Speciation of flightless rails on islands: a DNA-based phylogeny of the typical rails of the Pacific. Auk 129 , 56 – 69 . ( doi:10.1525/auk.2012.11259 ) 82 Wilson EO 1959 Adaptive shift and dispersal in a tropical ant fauna. Evolution 13 , 122 – 144 . ( doi:10.2307/2405948 ) 83 Pratt HD , Etpison MT 2008 Birds and bats of Palau. Honolulu, HI : Mutual Publishing L.L.C . 84 Olson SL 1973 Evolution of the rails of the South Atlantic islands (Aves: Rallidae). Smithson. Contrib. Zool. 152 , 1 – 53 . ( doi:10.5479/si.00810282.152 ) 85 Diamond JM 1981 Flightlessness and fear of flying in island species. Nature 293 , 507 – 508 . ( doi:10.1038/293507a0 ) 86 Komdeur J , Piersma T , Kraaijeveld K , Kraaijeveld-Smit F , Richardson DS 2004 Why Seychelles warblers fail to recolonize nearby islands: unwilling or unable to fly there? Ibis 146 , 298 – 302 . ( doi:10.1046/j.1474-919X.2004.00255.x ) 87 Berthold P , Helbig AJ , Mohr G , Querner U 1992 Rapid microevolution of migratory behaviour in a wild bird species. Nature 360 , 668 – 670 . ( doi:10.1038/360668a0 ) 88 Helbig AJ 1994 Genetic basis and evolutionary change of migratory directions in a European passerine migrant Sylvia atricapilla. Ostrich 65 , 151 – 159 . ( doi:10.1080/00306525.1994.9639677 ) 89 Pulido F 2007 The genetics and evolution of avian migration. BioScience 57 , 165 – 174 . ( doi:10.1641/B570211 ) 90 Gauthreaux SA 1982 The ecology and evolution of avian migration systems . In Avian biology (eds Farner DS , King JR and Parkes KC ), pp. 93 – 168 . New York, NY : Academic Press . 91 Winger BM , Lovette IJ , Winkler DW 2012 Ancestry and evolution of seasonal migration in the Parulidae. Proc. R. Soc. B 279 , 610 – 618 . ( doi:10.1098/rspb.2011.1045 ) 10.1098/rspb.2011.1045 PMC3234563 21752818 92 Winger BM , Barker FK , Ree RH 2014 Temperate origins of long-distance seasonal migration in New World songbirds. Proc. Natl Acad. Sci. USA 111 , 12115 – 12120 . ( doi:10.1073/pnas.1405000111 ) 25092321 10.1073/pnas.1405000111 PMC4143041