Phylogeography of the Variable Dwarf- lepidus (Aves: Alcedinidae) Inferred from Mitochondrial and Nuclear DNA Sequences Author(s): Michael J. Andersen , Carl H. Oliveros , Christopher E. Filardi , and Robert G. Moyle Source: The Auk, 130(1):118-131. 2013. Published By: The American Ornithologists' Union URL: http://www.bioone.org/doi/full/10.1525/auk.2012.12102

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PHYLOGEOGRAPHY OF THE VARIABLE DWARF-KINGFISHER CEYX LEPIDUS (AVES: ALCEDINIDAE) INFERRED FROM MITOCHONDRIAL AND NUCLEAR DNA SEQUENCES

MICHAEL J. ANDERSEN,1,3 CARL H. OLIVEROS,1 CHRISTOPHER E. FILARDI,2 AND ROBERT G. MOYLE1

1Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Lawrence, Kansas 66045, USA; and 2Center for Biodiversity and Conservation, American Museum of Natural History, New York, New York 10024, USA

Abstract.—We reconstructed the phylogeographic relationships of the Variable Dwarf-Kingfisher (Ceyx lepidus) using DNA sequence data. Maximum likelihood and Bayesian analysis methods were used to reconstruct trees from a multilocus data set of all  named subspecies of the Ceyx lepidus complex. The concatenated data-set length was , base pairs and included two mitochondrial genes and two noncoding nuclear introns. Support for the monophyly of C. lepidus was equivocal. We instead found support for a clade including all C. lepidus subspecies plus two endemic Philippine taxa: C. argentatus and C. cyanopectus. Relationships among subspecific taxa were not well resolved, and many nodes were collapsed into polytomies suggesting a rapid and widespread colonization. In situ diversification likely played a role in generating current diversity within four archipelagos: the Philippines, Malukus, Bismarcks, and Solomons. Some biogeographic patterns recovered for the Solomon Islands taxa match those seen in other species, such as the close relationship of taxa on Bougainville, Choiseul, and Isabel. By contrast, the sister relationship between populations on Guadalcanal and the New Georgia Group is novel. We discuss species limits and make taxonomic recommendations to treat all  subspecies of C. lepidus as species. Received  May , accepted  November .

Key words: biogeography, kingfisher, Philippines, Solomon Islands, species limits, western Pacific islands.

Phylogéographie de Ceyx lepidus (Aves : Alcédinidés inférée à partir de séquences d’adn mitochondrial et nucléaire

Résumé.—Nous avons reconstruit les relations phylogéographiques de Ceyx lepidus à l’aide de données de séquences d’ADN. Les méthodes du maximum de vraisemblance et d’inférence bayésienne ont été utilisées pour reconstruire les arbres à partir d’un ensemble de données multiloculaires des  sous-espèces du complexe d’espèces de Ceyx lepidus. La longueur concaténée de l’ensemble de données était de   paires de bases et incluait deux gènes mitochondriaux et deux introns nucléaires non codants. Les résultats appuyant la monophylie de C. lepidus étaient équivoques. Nous avons plutôt trouvé que les résultats suggéraient un clade comprenant toutes les sous-espèces de C. lepidus ainsi que deux taxons philippins endémiques, soit C. argentatus et C. cyanopectus. Les relations entre les taxons des sous-espèces n’ont pas bien été résolues et plusieurs nœuds ont été regroupés en polytomies, suggérant une colonisation rapide et étendue. La diversification in situ a vraisemblablement joué un rôle dans la génération de la diversité actuelle dans les quatre archipels : les Philippines, les Moluques, l’archipel Bismarck et les îles Salomon. Certains modèles biogéographiques pour les taxons des îles Salomon concordent avec ceux observés chez d’autres espèces d’oiseaux, tels que la relation étroite entre les taxons de Bougainville, Choiseul, et Isabel. En revanche, la relation fraternelle entre les populations de Guadalcanal et de Nouvelle-Géorgie est nouvelle. Nous discutons des limites spécifiques et faisons des recommandations taxonomiques pour traiter les  sous-espèces de C. lepidus comme des espèces.

The islands of Southeast Asia and the western Pacific are home Peterson ). These hyperdiverse species have served as exem- to some of the most phenotypically diverse avian species com- plars for ornithologists and biogeographers studying evolutionary plexes in the world. such as the Island Thrush Turdus( po- processes that lead to geographic partitioning of biological diver- liocephalus), Golden Whistler (Pachycephala pectoralis), and sity on islands (Mayr and Diamond ). Collared Kingfisher (Todiramphus chloris) are well known for The Variable Dwarf-Kingfisher Ceyx( lepidus) is another their widespread geographic distributions and diverse pheno- widespread, phenotypically diverse species that has long puzzled types, each having > subspecies (Galbraith , Woodall , ornithologists. Ceyx lepidus is a highly variable species with 

3E-mail: [email protected]

The Auk, Vol. , Number , pages −. ISSN -, electronic ISSN -. ©  by The American Ornithologists’ Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals. com/reprintInfo.asp. DOI: ./auk.. — 118 — JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —119

recognized subspecies (Fry et al. , Woodall , Clements meeki, and C. l. gentianus to be phenotypically disparate enough et al. ). Indeed, within its more limited distribution, C. lepi- to warrant status as so-called “megasubspecies.” Ceyx l. gentia- dus is nearly as diverse as the more widespread species complexes nus, for example, is the only taxon with a fully white breast and cited above (Clements et al. ). Each subspecies is defined by a C. l. dispar is the only one with sexually dichromatic plumage distinctive phenotype based on variation in breast, mantle, and (Fry et al. ). Notable plumage patterns also occur in the poly- rump coloration and bill color and shape. Subspecies are distrib- morphic Philippine endemic subspecies, C. l. margarethae, which uted allopatrically on islands from the Philippines to the Solomon has sympatric pale- and dark-backed morphs similar to the poly- Islands, including the Maluku Archipelago, New Guinea, and the morphism described in C. erithacus of mainland Southeast Asia Bismarck Archipelago (Fig. ). Ceyx lepidus is a biogeographic and the Sunda Shelf (Lim et al. ). In addition to plumage enigma; no other bird species shares its distribution. Indeed, no variation, bill structure and coloration vary dramatically within biogeographic term exists to circumscribe this region (Lomo- C. lepidus. Bills are either red or black; red bills tend to be lino et al. ). Interestingly, among terrestrial vertebrates, this dorsoventrally compressed, and black bills tend to be laterally com- distribution is mirrored closely by frogs in the genus Platyman- pressed. Two taxa, C. l. nigromaxilla and C. l. sacerdotis, have in- tis (Allison , Duellman ); however, Platymantis extends termediate bill colors with black or dusky maxillae and orange east to Fiji, whereas the Solomon Islands mark the eastern bound- mandibles (Fry et al. , Woodall ). Indeed, the amount of ary of C. lepidus. variation expressed in C. lepidus bill morphology matches that seen The general plumage pattern ofC. lepidus is blue or black across the entire clade to which it belongs: the pygmy-kingfishers above and rufous below. The breast and belly generally are ru- (subfamily Alcedininae). fous with a paler throat; the crown, back, wings, rump, and tail are Few attempts have been made to elucidate the phylogenetic blue or black; and a rufous loral spot and pale post-auricular stripe relationships of C. lepidus with other pygmy-kingfishers. Fry are present. Mayr and Diamond () considered close relation- () hypothesized a closer relationship with the Philippine en- ships among some subspecies based on these generalized plum- demic C. argentatus than with the sympatric C. melanurus based age patterns; however, they considered Ceyx lepidus dispar, C. l. on plumage characters. More recently, studies using molecular

FIG. 1. Map showing the distribution of the 15 subspecies of Ceyx lepidus in the Philippines, Wallacea, New Guinea, and Melanesia. Inset panel de- picts the distribution of closely related Philippine endemic species C. argentatus, C. cyanopectus, and C. melanurus. Black dots represent sampling localities used in this study; some dots represent more than one individual per locality. The reader is referred to Table 1 for the complete sampling list. The phylogeny is a cartoon of Figure 2 for topological reference. Black circles on nodes denote Bayesian posterior probability = 0.95 and maximum likelihood bootstrap support ≥70. 120 — ANDERSEN ET AL. — AUK, VOL. 130

data recovered C. lepidus in a well-supported clade of three- with ethidium bromide, and purified with % Exo-SAP-IT (GE toed pygmy-kingfishers in the genus Ceyx (Moyle , Moyle Healthcare Bio-Sciences, Piscataway Township, New Jersey). We et al. ) that included C. cyanopectus, C. argentatus, C. mel- cycle-sequenced purified PCR products in both directions with anurus, and C. erithacus. Furthermore, Moyle et al. () found the same primers used in PCR for  cycles, using the ABI Big Dye evidence of a paraphyletic C. lepidus, but the extent of paraphyly Terminator Cycle-Sequencing Kit, version . (Applied Biosys- was not known, owing to sampling deficiencies. Traditional tax- tems, Foster City, California). Sequencing was performed on an onomy, based largely on plumage characters and operating within ABI Prism  high-throughput capillary electrophoresis DNA the confines of the biological species concept, has for a long time analyzer and aligned sequences by hand using SEQUENCHER, treated C. lepidus as one species with  diagnosable subspecies version . (GeneCodes, Ann Arbor, Michigan). Nuclear intron (Peters , Clements et al. ). However, historically,  of alignments were done by hand and checked against an automated the  taxa were described as species (all except C. l. uropygialis, alignment in MUSCLE (Edgar ). C. l. mulcatus, C. l. pallidus, C. l. collectoris, C. l. malaitae, and Phylogenetic analysis and topology tests.—Phylogenetic C. l. nigromaxilla). Here, we reconstruct a molecular phylogeny reconstruction was performed both on the concatenated data of the C. lepidus species group and its closely related taxa in order and on each individual locus. Maximum likelihood (ML) tree to elucidate the evolutionary history and assess species limits of searches were performed using GARLI, version . (Zwickl ), this group. following the recommended default settings. We conducted , nonparametric bootstrap replicates (Felsenstein ) to assess METHODS clade credibility. We used SUMTREES, version ..—part of the DENDROPY, version .., package (Sukumaran and Holder Taxon sampling.—Ingroup sampling included all  named taxa )—to create bootstrap consensus trees and calculate bootstrap of C. lepidus (Clements et al. ) as well as representative sub- values. Models of DNA sequence evolution for all phylogenetic species of C. erithacus, C. melanurus, C. cyanopectus,and C. ar- analyses were tested using Akaike’s information criterion (AIC) gentatus ( of ,  of ,  of , and  of , respectively; Table ). employed in JMODELTEST, version .. (Guindon and Gascuel Outgroup sampling included all remaining taxa in the three-toed , Darriba et al. ). pygmy-kingfisher clade as circumscribed by Moyle et al. () Bayesian analysis (BA) was conducted using MRBAYES, ver- and websteri, which was used to root trees. We sequenced sion .. (Ronquist and Huelsenbeck , Altekar et al. , – individuals per taxon, but, whenever possible, more than one Ronquist et al. ) implemented with BEAGLE (Ayres et al. sample per taxon was used to guard against errors of misidentifi- ). The data were partitioned by codon position for mtDNA cation, mislabeling, or sample contamination. and by gene for the nuclear introns. Two independent MCMC runs DNA sequencing.—Total genomic DNA was extracted from of  million generations were conducted using default number of frozen or alcohol-preserved muscle tissue using a Qiagen tissue chains (n = ) and heating conditions, sampling every , gen- extraction protocol (Qiagen, Valencia, California). All tissue sam- erations. TRACER, version . (Rambaut and Drummond ), ples have associated museum study-skin vouchers. For taxa with and AWTY (Wilgenbusch et al. , Nylander et al. ) were no available tissue samples, DNA was extracted from toepads of used to assess convergence of parameter estimates and tree splits, museum study skins (Table ) in lab space separate from other respectively. The average standard deviation of split frequencies Ceyx tissue extractions to minimize contamination risk (Mundy (ASDSF) was used to determine topology convergence between et al. ). runs. The appropriate burn-in generations (% for all analyses) We sequenced the entire second and third subunits of mi- were discarded based on convergence assessments of the ASDSF tochondrial nicotinamide adenine dinucleotide dehydrogenase passing below .. The remaining trees were summarized in a (hereafter ND and ND, respectively), the second intron of the % majority-rule consensus tree. nuclear myoglobin gene (hereafter Myo), and the th intron Finally, the monophyly of C. lepidus was evaluated using the of the nuclear glyceraldehyde--phosphate dehydrogenase gene approximately unbiased (AU) test (Shimodaira ). Using the (hereafter GAPDH). Target DNA fragments were amplified us- same settings as the GARLI analyses described above,  ML ing polymerase chain reaction (PCR) with external and internal searches were performed,  unconstrained and  with a to- primers. ND and Myo primers are described by Moyle () pological constraint of C. lepidus monophyly. Per-site likelihoods and Moyle et al. (). Additionally, we used internal prim- were estimated for each tree under a partitioned model, and an AU ers L (Oliveros and Moyle ) and H (designed for this test was performed on these values using CONSEL, version .i project; ′-GATRATAATRGCYATTCAKCC-′) to amplify ND (Shimodaira and Hasegawa ). TheP value reported is the larg- and the internal primer KingMyoR (′-AGGTTGCAGAGCC est P value of all trees inferred under the constraint. TGGAAATATCTC-′) to amplify Myo on some samples. The primer combinations L and H (Chesser ) and RESULTS GPb and GPb (Fjeldså et al. ) were used to amplify ND and GAPDH, respectively. Sequence attributes.—The aligned data set was , base pairs The PCR amplifications were performed in -μL reac- (bp) and included  samples from  named taxa. All sequences tions using -PRIME HotMaster Taq DNA polymerase with a are deposited in GenBank (accession nos. KC–KC). touchdown protocol for mtDNA and GAPDH (annealing tem- We obtained DNA sequences for all genes for all samples, with perature: , , and °C). We used an annealing temperature the exception of those taken from museum skins, for which we of °C for Myo following Kimball et al. (). Amplified PCR were only able to sequence mitochondrial genes (Table ). Align- products were screened on high-melt, % agarose gels stained ment lengths were , bp (ND),  bp (ND),  bp (Myo), JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —121

TABLE 1. Samples used to reconstruct the phylogeny of Ceyx lepidus, including voucher institution and locality.

Taxon Voucher a Sample number Locality

Alcedo hercules d KUNHM 10160 China: Guangxi Province Ceyx azureus KUNHM 96095 Papua New Guinea: Gulf Province C. fallax b,d,e AMNH 299259 Indonesia: Sulawesi C. pusillus UWBM Bu67896 Solomon Islands: Western Province, New Georgia Island C. websteri USNM 608680f Papua New Guinea: Bismarck Archipelago C. argentatus argentatus KUNHM 18103 Philippines: Mindanao Island C. a. argentatus KUNHM 19071 Philippines: Mindanao Island C. a. argentatus KUNHM 19252 Philippines: Mindanao Island C. a. argentatus KUNHM 19268 Philippines: Mindanao Island C. a. argentatus KUNHM 19269 Philippines: Mindanao Island C. a. flumenicolus KUNHM 14284 Philippines: Leyte Island C. a. flumenicolus KUNHM 14289 Philippines: Leyte Island C. a. flumenicolus KUNHM 14241 Philippines: Samar Island C. cyanopectus cyanopectus KUNHM 17990 Philippines: Luzon Island C. c. cyanopectus KUNHM 18068 Philippines: Luzon Island C. c. cyanopectus KUNHM 20334 Philippines: Luzon Island C. erithacus erithacus KUNHM 10417 China: Guangxi Province C. e. motleyi LSUMNS B38586 Malaysia: Borneo, Sabah C. e. motleyi KUNHM 12359 Malaysia: Borneo, Sarawak C. e. motleyi c,d KUNHM 12650 Philippines: Palawan Island C. e. motleyi c,d KUNHM 12808 Philippines: Palawan Island C. lepidus cajeli b,c,d,e AMNH 637134 Indonesia: Maluku Province, Buru Island C. l. collectoris d UWBM Bu66054 Solomon Islands: Western Province, New Georgia Island C. l. collectoris d UWBM Bu68064 Solomon Islands: Western Province, New Georgia Island C. l. collectoris UWBM Bu68077 Solomon Islands: Western Province, New Georgia Island C. l. dispar KUNHM 5611 Papua New Guinea: Manus Province, Manus Island C. l. gentianus KUNHM 12801 Solomon Islands: Makira-Ulawa Province: Makira Island C. l. gentianus KUNHM 13530 Solomon Islands: Makira-Ulawa Province: Makira Island C. l. gentianus KUNHM 13540 Solomon Islands: Makira-Ulawa Province: Makira Island C. l. lepidus b,c,d,e AMNH 637099 Indonesia: Maluku Province, Ambon Island C. l. malaitae UWBM Bu66025 Solomon Islands: Malaita Province: Malaita Island C. l. margarethae KUNHM 14022 Philippines: Camiguin Sur Island C. l. margarethae KUNHM 14031 Philippines: Camiguin Sur Island C. l. margarethae KUNHM 14355 Philippines: Camiguin Sur Island C. l. margarethae KUNHM 14384 Philippines: Camiguin Sur Island C. l. margarethae KUNHM 14397 Philippines: Camiguin Sur Island C. l. margarethae KUNHM 19259 Philippines: Mindanao Island C. l. margarethae FMNH 344953 Philippines: Sibuyan Island C. l. margarethae FMNH 358316 Philippines: Sibuyan Island C. l. margarethae FMNH 358317 Philippines: Sibuyan Island C. l. margarethae KUNHM 14484 Philippines: Tablas Island C. l. margarethae KUNHM 14485 Philippines: Tablas Island C. l. meeki UWBM Bu63203 Solomon Islands: Choiseul Province, Choiseul Island C. l. meeki c,d UWBM Bu60194 Solomon Islands: Isabel Province, Isabel Island C. l. meeki AMNH DOT6641 Solomon Islands: Isabel Province, Isabel Island C. l. mulcatus e LACM 91032 Papua New Guinea: New Ireland Province, New Ireland Island C. l. mulcatus d,e LACM 91033 Papua New Guinea: New Ireland Province, New Ireland Island C. l. mulcatus b,c,d,e AMNH 335499 Papua New Guinea: New Ireland Province, Tabar Island C. l. nigromaxilla KUNHM 15880 Solomon Islands: Guadalcanal Province, Guadalcanal Island C. l. nigromaxilla KUNHM 15892 Solomon Islands: Guadalcanal Province, Guadalcanal Island C. l. nigromaxilla UWBM Bu60341 Solomon Islands: Guadalcanal Province, Guadalcanal Island C. l. pallidus KUNHM 5633 Papua New Guinea: Bougainville Province, Bougainville Island C. l. sacerdotis UWBM Bu67945 Papua New Guinea: West New Britain Province, ~12 km SE Talasea C. l. sacerdotis UWBM Bu68050 Papua New Guinea: West New Britain Province, ~12 km SE Talasea C. l. solitarius KUNHM 5157 Papua New Guinea: Chimbu Province C. l. solitarius UWBM Bu68037 Papua New Guinea: Chimbu Province C. l. solitarius KUNHM 9539 Papua New Guinea: East Sepik Province C. l. solitarius KUNHM 5192 Papua New Guinea: Gulf Province, Ivimka Camp C. l. solitarius UWBM Bu67992 Papua New Guinea: Gulf Province, Ivimka Camp C. l. solitarius UWBM Bu68021 Papua New Guinea: Gulf Province, Ivimka Camp C. l. solitarius d KUNHM 7229 Papua New Guinea: Madang Province (continued) 122 — ANDERSEN ET AL. — AUK, VOL. 130

TABLE 1. Continued

Taxon Voucher a Sample number Locality

C. l. solitarius KUNHM 7295 Papua New Guinea: Madang Province C. l. solitarius KUNHM 6977 Papua New Guinea: Oro Province C. l. solitarius KUNHM 6982 Papua New Guinea: Oro Province C. l. solitarius KUNHM 7526 Papua New Guinea: Western Province C. l. uropygialis e YPM 74993 Indonesia: North Maluku Province, Bacan Island C. l. uropygialis d,e YPM 74989 Indonesia: North Maluku Province, Halmahera Island C. l. uropygialis b,c,d,e AMNH 637110 Indonesia: North Maluku Province, Halmahera Island C. l. wallacii b,c,d,e AMNH 637152 Indonesia: North Maluku Province, Mangole Island C. melanurus melanurus KUNHM 18046 Philippines: Luzon Island C. m. melanurus KUNHM 20203 Philippines: Luzon Island C. m. mindanensis KUNHM 18184 Philippines: Mindanao Island C. m. mindanensis KUNHM 19006 Philippines: Mindanao Island C. m. samarensis KUNHM 14304 Philippines: Leyte Island C. m. samarensis KUNHM 14226 Philippines: Samar Island

a Institutional abbreviations for voucher sources are as follows: AMNH = American Museum of Natural History; FMNH = Field Museum of Natural History; KUNHM = University of Kansas Natural History Museum; LACM = Los Angeles County Museum; LSUMNS = Louisiana State University Museum of Natural Science; UWBM = Burke Museum, University of Washington; USNM = National Museum of Natural History, Smithsonian Institution; and YPM = Yale Peabody Museum. b,c,d Denotes samples for which data are lacking from ND3, Myo2, and/or GAPDH, respectively. e Denotes samples for which DNA was extracted from museum study skins. f This sample is the same as “B04021” from Moyle et al. (2007). and  bp (GAPDH). The aligned data set contained  variable outgroup taxa (C. erithacus and C. melanurus) and the ingroup characters (.%) and  (.%) parsimony-informative char- clade (Fig. , clade A), which comprised C. lepidus, C. cyanopectus, acters. Pairwise distances in ND (uncorrected p; Table ) ranged and C. argentatus. However, relationships among C. erithacus, .–.% between outgroup taxa and C. lepidus and .–.% C. melanurus, and clade A were unresolved, a result similar to (mean = .%) among C. lepidus taxa. those obtained by Moyle et al. () and Lim et al. (). The sy- The ND gene sequence contained a single cytosine insertion napomorphic indel observed in the GAPDH intron supports a sis- at position  in all samples, an insertion reported in several other ter relationship between C. melanurus and C. erithacus, but this bird groups and turtles (Mindell et al. ). This insertion does not hypothesis requires further investigation. disrupt the reading frame because it is not translated. Apart from this Support for clade A was unequivocal, but monophyly of insertion in ND, the mitochondrial data showed no other insertions, C. lepidus received no support. Instead, basal relationships deletions, or anomalous stop-codons; thus, there was no evidence within clade A consisted of a polytomy among four well-sup- that mtDNA sequences were of nuclear origin (i.e., pseudogenes; ported clades: () the Philippine endemics C. cyanopectus and Sorenson and Quinn ). The relative divergence among codon C. argentatus (Fig. , clade B); () Wallacean C. l. cajeli and C. l. positions was typical for mtDNA ( >  > ). Four deletions were wallacii (Fig. , clade C); () Philippine endemic C. l. margarethae noted in Myo, but all were autapomorphic in the following samples: (Fig. , clade D); and () a clade including the remaining  subspe- C. pusillus ( bp), C. erithacus ( bp in each: B and ), and cies of C. lepidus (Fig. , clade E). Although the polytomy raised C. l. margarethae ( bp; ). A synapomorphic -bp deletion was the possibility that C. lepidus is paraphyletic, this relationship shared by all C. erithacus and C. melanurus samples in GAPDH. On is best considered unresolved. Indeed, an AU test failed to reject the basis of model testing results, we used the GTR+I+G model of C. lepidus monophyly (P = .). Despite the lack of resolution at sequence evolution for all three mtDNA codon positions, HKY+I for the bases of Clades A and E, each of the  C. lepidus subspecies Myo, and HKY+G for GAPDH. All ML analyses with GARLI were was monophyletic, and several sister pairs were well supported: done with the GTR+I+G model across the entire data set. C. l. mulcatus + C. l. solitarius, C. l. collectoris + C. l. nigromaxilla, Phylogenetic relationships.—Individual gene trees were highly and C. l. pallidus + C. l. meeki. concordant (Fig. ). The topologies recovered from analyses of Within C. argentatus phylogeographic structure was con- mtDNA showed greater resolution than those derived from nuclear cordant with named subspecies (discussed below). Conversely, introns, which was expected given the higher rates of sequence evo- we found no discernible genetic structure within two wide- lution in mtDNA compared with nuclear DNA (Brown et al. spread C. lepidus subspecies: C. l. margarethae and C. l. solitar- ). No well-supported clades recovered from the analysis of in- ius, despite broad sampling within their ranges. This result was dividual genes conflicted with those from other gene trees or those somewhat expected for C. l. solitarius and likely suggests a high from the concatenated data set, so we focused our discussion on amount of gene flow across the island of New Guinea. However, phylogenetic relationships inferred from the concatenated data set the lack of genetic differentiation in C. l. margarethae across (Fig. ). The inferred topologies from multiple independent ML and multiple Philippine oceanic islands—and representing two color BA runs were highly concordant. The best ML topology had a –ln morphs—is noteworthy. likelihood score of ., as reported in GARLI. Finally, removal of the five taxa represented by only one gene We recovered a well-supported clade (i.e., Bayesian poste- sequence in our data set (C. l. dispar, C. l. malaitae, C. l. cajeli, rior probability >% and ML bootstrap >%) that included two C. l. wallacii, and C. l. lepidus) had little effect on results of JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —123

TABLE 2. Uncorrected ND2 pairwise p-distances. Mean pairwise distances are reported for taxa with more than one sample. Column headers are abbreviated with the first three letters of the subspecific epithet.

eri. mot. mel. min. sam. arg. flu. cya. caj. col. dis. gen.

C. erithacus erithacus — C. e. motleyi 0.048 — C. melanurus melanurus 0.088 0.085 — C. m. mindanensis 0.085 0.076 0.026 — C. m. samarensis 0.084 0.084 0.019 0.025 — C. argentatus argentatus 0.085 0.080 0.070 0.065 0.070 — C. a. flumenicolus 0.092 0.083 0.074 0.070 0.077 0.025 — C. cyanopectus cyanopectus 0.092 0.080 0.072 0.068 0.073 0.034 0.041 — C. lepidus cajeli 0.080 0.075 0.059 0.056 0.060 0.045 0.046 0.054 — C. l. collectoris 0.098 0.088 0.084 0.079 0.084 0.062 0.064 0.069 0.057 — C. l. dispar 0.089 0.083 0.073 0.068 0.077 0.057 0.058 0.059 0.045 0.065 — C. l. gentianus 0.092 0.088 0.073 0.066 0.080 0.054 0.057 0.063 0.041 0.067 0.053 — C. l. lepidus 0.086 0.082 0.069 0.064 0.065 0.045 0.050 0.057 0.047 0.063 0.055 0.057 C. l. malaitae 0.093 0.088 0.075 0.070 0.081 0.059 0.061 0.059 0.053 0.061 0.057 0.054 C. l. margarethae 0.086 0.080 0.073 0.066 0.073 0.055 0.064 0.063 0.046 0.061 0.062 0.062 C. l. meeki 0.085 0.085 0.074 0.067 0.077 0.056 0.060 0.061 0.047 0.068 0.056 0.063 C. l. mulcatus 0.099 0.086 0.077 0.067 0.078 0.062 0.062 0.063 0.052 0.067 0.062 0.052 C. l. nigromaxilla 0.094 0.089 0.078 0.071 0.081 0.061 0.064 0.065 0.048 0.053 0.059 0.059 C. l. pallidus 0.083 0.083 0.076 0.068 0.080 0.052 0.062 0.062 0.049 0.070 0.060 0.061 C. l. sacerdotis 0.100 0.092 0.076 0.073 0.082 0.060 0.061 0.069 0.047 0.073 0.061 0.051 C. l. solitarius 0.093 0.085 0.078 0.073 0.082 0.066 0.067 0.070 0.044 0.066 0.065 0.054 C. l. uropygialis 0.089 0.082 0.071 0.067 0.077 0.051 0.052 0.061 0.051 0.065 0.058 0.054 C. l. wallacii 0.083 0.076 0.062 0.058 0.061 0.050 0.048 0.058 0.016 0.061 0.054 0.048

lep. mal. mar. mee. mul. nig. pal. sac. sol. uro. wal.

C. l. lepidus — C. l. malaitae 0.056 — C. l. margarethae 0.060 0.064 — C. l. meeki 0.045 0.053 0.062 — C. l. mulcatus 0.060 0.058 0.060 0.060 — C. l. nigromaxilla 0.058 0.056 0.064 0.057 0.058 — C. l. pallidus 0.051 0.050 0.062 0.032 0.060 0.068 — C. l. sacerdotis 0.061 0.060 0.067 0.063 0.060 0.063 0.066 — C. l. solitarius 0.060 0.061 0.066 0.064 0.033 0.065 0.068 0.063 — C. l. uropygialis 0.048 0.056 0.060 0.057 0.055 0.063 0.053 0.062 0.061 — C. l. wallacii 0.052 0.056 0.050 0.052 0.056 0.060 0.053 0.048 0.054 0.055 —

Bayesian analysis of the concatenated data set. Bayesian poste- pattern of rapid and widespread colonization across Southeast Asia rior probabilities and the backbone topology were extremely simi- and the Pacific islands is thought to have occurred in other wide- lar between analyses with and without the five taxa (results not spread polytypic species complexes such as Todiramphus chlo- shown). ris, Pachycephala pectoralis, and Turdus poliocephalus (Mayr and Diamond ). However, densely sampled phylogenetic hypothe- DISCUSSION ses are not available to test this hypothesis in these groups (but see Jones and Kennedy b, Jønsson et al ). Biogeography.—Here, we present the first fully sampled molecular The highest diversity in this group of dwarf-kingfishers (un- phylogeny of Ceyx lepidus. Although the abundance of unresolved der present ) occurs in the Philippine archipelago, where relationships precluded quantitative biogeographic analysis, some one to three species are present on each major island. It appears biogeographic insights are evident from our results. that in situ diversification of C. argentatus and C. cyanopectus Overall, the most striking aspect of the phylogeny is that each (clade B) in the Philippines played a role in generating this diver- taxon in the C. lepidus complex is monophyletic and substantially sity. Our results also indicate that multiple colonization events diverged from all other taxa (.–.% divergent in uncorrected contributed to the diversity of dwarf-kingfishers in the Philip- ND p-distance). We interpret this pattern of shallow internodes pines; the ancestors of C. erithacus appear to have invaded the at the base, long stem lineages, and shallow divergences within each western Philippines from the Sunda Shelf, and at least two other taxon as support for a scenario in which C. lepidus achieved its full colonization events were responsible for the presence of C. mela- geographic distribution rapidly, followed by little or no subsequent nurus, C. cyanopectus, C. argentatus, and C. l. margarethae in the gene flow among most island populations. This biogeographic archipelago. These four taxa occur in sympatry on some islands, 124 — ANDERSEN ET AL. — AUK, VOL. 130 es es 70. Numbers by nodes indicate Bayesian PP. Some from trees taxa are missing B and C because data PP. Numbers nodes Bayesian by 70. indicate ≥ complex for each of the three independently segregating loci: (A) mtDNA: ND2+ND3, (B) Myo2, and (C) GAPDH. Black circles on nod of the for each three and (C)complex (B) circles independently segregating loci: (A) mtDNA: GAPDH. Myo2, Black ND2+ND3, Ceyx lepidus lepidus Ceyx Bayesian phylogenies of the phylogenies Bayesian . 2. IG are lacking for Myo2 and GAPDH, respectively. for Myo2 are lacking denote Bayesian posterior probability = 0.95 and maximum likelihood bootstrap and maximum likelihood support posterior = 0.95 probability denote Bayesian F JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —125

FIG. 3. Bayesian phylogeny of the Ceyx lepidus complex based on a concatenated data set of two mitochondrial coding genes and two nuclear introns. Black circles on nodes denote Bayesian posterior probability (PP) = 0.95 and maximum likelihood (ML) bootstrap support ≥70. Numbers by nodes detail unresolved nodes, with numbers above branches indicating Bayesian PP and those below branches ML bootstrap. 126 — ANDERSEN ET AL. — AUK, VOL. 130

but it is uncertain whether they occur syntopically. For instance, but we did not recover genetic structure in C. l. margarethae with C. argentatus, C. melanurus,and C. l. margarathae all occur on respect to geography or plumage polymorphism. Recent stud- Mindanao, and although natural history data are sparse for these ies have found that single point mutations in the melanocortin- taxa, preliminary observations suggest that C. argentatus is a -receptor gene are associated with plumage polymorphisms in stream-associated species, whereas C. melanurus and C. l. marga- Bananaquits (Coereba flaveola) and monarchs (Monarchidae; rethae are forest species with no affinity to water (P. Hosner pers. Theron et al. , Uy et al. b). It is possible that a single point comm.). This pattern suggests that at least some level of ecologi- mutation is driving plumage polymorphism in C. l. margarethae, cal partitioning helps separate these otherwise broadly sympatric and investigations on the role of this gene in polymorphism in taxa. Ceyx species are recommended. Some geographic insight can be gleaned from sister The subspecies C. l. dispar, from the Admiralty Islands of relationships in the C. lepidus species group. For instance, dwarf Papua New Guinea, is sexually dichromatic—the male has the kingfishers of the Malukus are derived from two well-supported typical blue head, whereas the female is orange-headed. This pat- but unrelated pairs of sister taxa (C. l. cajeli and C. l. wallacii; tern is reminiscent of the pygmy-kingfishers of Africa C. l. lepidus and C. l. uropygialis), which indicates the combined (Fry et al. ). Only one other ingroup taxon, C. cyanopectus, is role of colonization and local diversification in generating diver- sexually dichromatic; males have a double breast band, whereas sity. In situ diversification is also evident in the Solomon Islands females have only one breast band (Kennedy et al. ). Sexual with the recovery of two pairs of sister taxa within the island dichromatism thus appears to have evolved twice in the ingroup. group. The first pair,C. l. pallidus and C. l. meeki, reflects the close Indeed, other instances of differential patterns of sexual dichro- affinities of Bougainville, Choiseul, and Isabel, which form part matism in polytypic insular bird species are known. For example, of the Pleistocene island of Greater Bukida (Mayr and Diamond Turdus poliocephalus niveiceps and T. p. carbonarius are sexually ). The close affinity of fauna within Greater Bukida, especially dichromatic on Taiwan and New Guinea, respectively, but not between Choiseul and Isabel, is documented in multiple avian elsewhere (Peterson ). Interestingly, Pachycephala pectora- lineages (Smith and Filardi , Uy et al. a) and also has lis feminina on Rennell Island in the Solomon Islands is sexually been observed in bats (Pulvers and Colgan ). Bougainville monochromatic; in this instance, the male reverts to female plum- tends to have taxa more divergent from the rest of the Greater age (Galbraith ). Bukida islands (Mayr and Diamond ), and this pattern is also Taxonomy.—Our discussion of taxonomy is based largely seen in Ceyx. The second sister pair within the Solomon Islands, on an evolutionary species concept (Simpson , Wiley C. l. collectoris and C. l. nigromaxilla, reveals a close relationship ) and its extension, the general lineage-based species con- between the New Georgia Group and Guadalcanal, a biogeo- cept (de Queiroz ). We draw upon details of genetic di- graphic pattern not recovered in other avian studies (Filardi and vergence, biogeography, and plumage pattern as the most Smith , Smith and Filardi , Uy et al. a). The mostly prescient evidence. Application of lineage-based species con- unresolved relationships among the lineages in clade E obscure cepts to island systems is preferable to the biological species the number of colonization events on the Solomon Islands. Lastly, concept (Mayr ) because reproductive isolation between the sister relationship of C. l. solitarius and C. l. mulcatus unites allopatric insular taxa cannot be assessed. Instead, we em- New Guinea with the northern Bismarck Archipelago islands of ploy a lineage-based species concept to recognize ancestor– New Ireland, New Hanover, Tabar, and Lihir. This result suggests descendant populations with unique evolutionary histories. that at least two independent colonization events were involved Two Philippine species warrant discussion on species lim- in assembling the dwarf-kingfishers of the Bismarcks. This sister its: C. argentatus and C. melanurus. Ceyx argentatus is distrib- pairing is cohesive with respect to plumage because they are uted throughout the central and southern Philippines (Fig. , inset). nearly identical—both are rufous below, with whitish throats, pale Two subspecies of C. argentatus are described: C. a. argentatus and rufous loral spots, dark blue backs, and black bills. This pattern of C. a. flumenicolus, though both were originally described as species similarly plumaged sister taxa was not upheld throughout the rest (Peters ). We recovered these two subspecies as sister clades di- of the tree, which highlights the need for revisionary taxonomy verged by .% ND uncorrected p-distances. Our results support the not based solely on plumage patterns in polytypic, insular species suggestion of Collar (), which was based on morphological data, complexes (Peterson ). to treat C. argentatus and C. flumenicolus as full species, but we ac- Plumage polymorphism.—Examples of plumage polymor- knowledge that this pair of taxa requires further investigation to de- phism in birds are numerous and have received much atten- termine whether there is gene flow between them. On the other hand, tion (Roulin ). Ceyx l. margarethae, an endemic of central C. melanurus consists of three subspecies, which are distributed along and southern Philippines, is the only C. lepidus subspecies for the eastern arc of the Philippines (Fig. , inset): C. m. melanurus, C. m. which polymorphism within single-island populations occurs. samarensis, and C. m. mindanensis. We sampled all three subspecies Ceyx erithacus is the only other Ceyx species to exhibit within and found strong support for the sister relationship of C. m. mindanen- population plumage polymorphism (Fry et al. ). Lim et al. sis and a clade comprising C. m. melanurus and C. m. samarensis. Mor- () found evidence for polymorphism in C. erithacus as a re- phologically, these forms differ in the extent of black on the wings and sult of admixture of historically separate and genetically well- the presence or absence of a blue streak on the side of the head (Fry et al. differentiated populations across Southeast Asia and the Sunda ). A comprehensive study of the genetic structure and morphologi- Shelf. We sampled widely throughout the range of C. l. margare- cal variation in this species is ongoing (P. Hosner unpubl. data); thus, thae, including pale- and dark-backed individuals from the Phil- we refrain from recommending taxonomic changes in this group. In ippine islands of Camiguin Sur, Tablas, Mindanao, and Sibuyan, both C. argentatus and C. melanurus, our data demonstrate the genetic JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —127

distinctiveness of species on the eastern Philippine islands of Samar, History; M. Robbins, University of Kansas Biodiversity Institute; Leyte, and Bohol, despite their land connection to Mindanao during K. Garrett, Los Angeles County Museum; D. Dittman, Louisiana the last glacial maximum. This result provides another example show- State University Museum of Natural Science; C. Milensky, National ing the distinctiveness of avian populations in this group of islands Museum of Natural History, Smithsonian Institution; S. Birks, (Sánchez-González and Moyle , Sheldon et al. ) and supports Burke Museum, University of Washington; and K. Zyskowski, Yale a nascent, but growing, body of studies in recognizing that the para- Peabody Museum. We are also grateful to the specimen collectors digm of late Pleistocene aggregate islands explaining the distribution whose efforts in the field helped make this project possible. H. Shult of diversity in the Philippines, as proposed by Heaney (), is overly assisted with molecular lab work at the University of Kansas, and simplistic for mammals, reptiles, amphibians, and birds (Evans et al. P. Hosner, R. Jones, J. Manthey, and two anonymous reviewers , Jones and Kennedy a, Esselstyn and Brown , Linkem et offered insightful comments on the manuscript. This work was al. , Oliveros and Moyle , Siler et al. ). supported by the National Science Foundation (DEB- to Plumage differences among the  C. lepidus subspecies were R.G.M.). For permission to undertake research in the Philippines, described by Fry et al. () and Woodall () and are summarized we thank the Department of Environment and Natural Resources in the Appendix. Below, we discuss in detail an example of highly diver- of the Philippines and the Protected Areas and Wildlife Bureau. gent plumage and an example in which the plumage differentiation is minimal, and the reader is referred to the Appendix for details of plum- LITERATURE CITED age differences that are not discussed in the text. Ceyx l. gentianus from Makira Island in the Solomon Islands is one of the most morphologically Allison, A. . Zoogeography of amphibians and reptiles of New disparate taxa. It is entirely white below, lacking the rufous tones found Guinea and the Pacific region. Pages – in The Origin and in most other forms of C. lepidus (Fry et al. , Dutson ). Other Evolution of Pacific Island Biotas, New Guinea to Eastern Polyne- described taxa have more subtle plumage differences, and the two most sia: Patterns and Processes (A. Keast and S. E. Miller, Eds.). SPB similar taxa occur in the Solomon Islands. The Bougainville taxon, Academic Publishing, Amsterdam. C. l. pallidus, one of the few taxa originally described as a subspe- Altekar, G., S. Dwarkadas, J. P. Huelsenbeck, and F. Ron- cies of C. lepidus, is slightly paler than C. l. meeki from Choiseul quist. . Parallel Metropolis-coupled Markov chain Monte and Isabel islands. In his description, Mayr () noted that C. l. Carlo for Bayesian phylogenetic inference. Bioinformatics pallidus is “similar to Ceyx lepidus meeki, but [its] under parts [are] :–. pale yellowish buff, instead of golden-yellowish ochre.” Ceyx l. pal- Ayres, D. L., A. Darling, D. J. Zwickl, P. Beerli, M. T. Holder, lidus appears to be only weakly differentiated from C. l. meeki in P. O. Lewis, J. P. Huelsenbeck, F. Ronquist, D. L. Swofford, plumage, but our data support a well-differentiated genetic split M. P. Cummings, and others. . BEAGLE: An application (.% ND uncorrected p-distance) between these sister taxa. This programming interface and high-performance computing library divergence is substantially higher than the .% divergence between for statistical phylogenetics. Systematic Biology :–. C. a. argentatus and C. a. flumenicolus, two morphologically divergent Brown, W. M., M. George, Jr., and A. C. Wilson. . Rapid sister taxa. It appears that in the case of C. l. pallidus and C. l. meeki, evolution of animal mitochondrial DNA. Proceedings of the morphology was conserved while their populations diverged. National Academy of Sciences USA :–. Although our phylogeny does not resolve the apparent rapid Chesser, R. T. . Molecular systematics of the rhinocryptid and widespread geographic diversification of C. lepidus in a bifur- genus Pteroptochos. Condor :–. cating fashion, it provides a basis for a reevaluation of species limits Clements, J. F., T. S. Schulenberg, M. J. Iliff, B. L. Sullivan, in this group. We propose recognizing all  C. lepidus subspecies C. L. Wood, and D. Roberson. . The Clements Checklist of as species for the following reasons: () each subspecies is morpho- Birds of the World, version .. [Online.] Available at www.birds. logically distinct; () these taxa exhibit a relatively uniform and high cornell.edu/clementschecklist/downloadable-clements-checklist. degree of genetic differentiation among lineages (.–.% in ND Collar, N. J. . Species limits in some Philippine birds including uncorrected p-distance; Table ), which is higher than in two sister the Greater Flameback Chrysocolaptes lucidus. Forktail :–. taxa (C. argentatus and C. flumenicolus) that are closely related to Darriba, D., G. L. Taboada, R. Doallo, and D. Posada. . C. lepidus; and () the  subspecies have allopatric distributions jModelTest : More models, new heuristics and parallel comput- and, therefore, are experiencing their own evolutionary fate. ing. Nature Methods :. Our results support an improved understanding of the high de Queiroz, K. . The general lineage concept of species and degree of morphologic and cryptic genetic diversity found not the defining properties of the species category. Pages – in only in Philippine birds (Lohman et al. ) but more broadly in Species: New Interdisciplinary Essays (R. A. Wilson, Ed.). Massa- the archipelagos of Southeast Asia and the Pacific. Recognizing chusetts Institute of Technology Press, Cambridge. subspecies of C. lepidus as full species will have important conser- Duellman, W. E., Ed. . Patterns of Distribution of Amphibians: vation implications, especially because most taxa are endemic to A Global Perspective. Johns Hopkins University Press, Baltimore, small islands or island groups. Maryland. Dutson, G. . Birds of Melanesia: Bismarcks, Solomons, Vanu- ACKNOWLEDGMENTS atu, and New Caledonia. Princeton University Press, Princeton, New Jersey. We thank the following museum curators and collection manag- Edgar, R. C. . MUSCLE: Multiple sequence alignment with ers for assistance with specimen loans: P. Sweet, American Mu- high accuracy and high throughput. Nucleic Acids Research seum of Natural History; D. Willard, Field Museum of Natural :–. 128 — ANDERSEN ET AL. — AUK, VOL. 130

Esselstyn, J. A., and R. M. Brown. . The role of repeated Linkem, C. W., K. M. Hesed, A. C. Diesmos, and R. M. Brown. sea-level fluctuations in the generation of shrew (Soricidae: Croc- . Species boundaries and cryptic lineage diversity in a Philip- idura) diversity in the Philippine Archipelago. Molecular Phylo- pine forest skink complex (Reptilia; Squamata; Scincidae: Lygoso- genetics and Evolution :–. minae). and Evolution :–. Evans, B. J., R. M. Brown, J. A. McGuire, J. Supriatna, Lohman, D. J., K. K. Ingram, D. M. Prawiradilaga, K. Winker, N. Andayani, A. Diesmos, D. Iskandar, D. J. Melnick, and F. H. Sheldon, R. G. Moyle, P. K. L. Ng, P. S. Ong, L. K. Wang, D. C. Cannatella. . Phylogenetics of fanged frogs: Testing T. M. Braile, and others. . Cryptic genetic diversity in biogeographical hypotheses at the interface of the Asian and Aus- “widespread” Southeast Asian bird species suggests that Philip- tralian faunal zones. Systematic Biology :–. pine avian endemism is gravely underestimated. Biological Con- Felsenstein, J. . Confidence limits on phylogenies: An servation :–. approach using the bootstrap. Evolution :–. Lomolino, M. V., B. R. Riddle, R. J. Whittaker, and J. H. Filardi, C. E., and C. E. Smith. . Molecular phylogenetics of Brown. . Biogeography, th ed. Sinauer Associates, Sunder- monarch flycatchers (genus Monarcha) with emphasis on Solo- land, Massachusetts. mon Island endemics. Molecular Phylogenetics and Evolution Mayr, E. . Birds collected during the Whitney South Sea Expe- :–. dition: Descriptions of twenty-five new species and subspecies. Fjeldså, J., D. Zuccon, M. Irestedt, U. S. Johansson, and P. G. P. American Museum Novitates :–. Ericson. . Sapayoa aenigma: A New World representative of Mayr, E. . Animal Species and Evolution. Harvard University ‘Old World suboscines.’ Proceedings of the Royal Society of Lon- Press, Cambridge, Massachusetts. don, Series B  (Supplement ):–. Mayr, E., and J. M. Diamond. . Birds of Northern Melanesia. Fry, C. H. . The evolutionary biology of kingfishers (Alcedini- Oxford University Press, New York. dae). Living Bird :–. Mindell, D. P., M. D. Sorenson, and D. E. Dimcheff. . Fry, C. H., K. Fry, and A. Harris. . Kingfishers, Bee-eaters, An extra nucleotide is not translated in mitochondrial ND and Rollers. Christopher Helm, London. of some birds and turtles. Molecular Biology and Evolution Galbraith, I. C. J. . Variation, relationships and evolution :–. in the Pachycephala pectoralis superspecies (Aves, Muscicapi- Moyle, R. G. . A molecular phylogeny of kingfishers (Alcedinidae) dae). Bulletin of the British Museum (Natural History) Zoology with insights into early biogeographic history. Auk :–. :–. Moyle, R. G., J. Fuchs, E. Pasquet, and B. D. Marks. . Guindon, S., and O. Gascuel. . A simple, fast, and accurate Feeding behavior, toe count, and the phylogenetic relationships algorithm to estimate large phylogenies by maximum likelihood. among alcedinine kingfishers (Alcedininae). Journal of Avian Systematic Biology :–. Biology :–. Heaney, L. R. . Biogeography of mammals in SE Asia: Esti- Mundy, N. I., P. Unitt., and D. S. Woodruff. . Skin from feet mates of rates of colonization, extinction and speciation. Biologi- of museum specimens as a non-destructive source of DNA for cal Journal of the Linnean Society :–. avian genotyping. Auk :–. Jones, A. W., and R. S. Kennedy. a. Evolution in a tropical Nylander, J. A. A., J. C. Wilgenbusch, D. L. Warren, and D. L. archipelago: Comparative phylogeography of Philippine fauna Swofford. . AWTY (are we there yet?): A system for graphi- and flora reveals complex patterns of colonization and diversi- cal exploration of MCMC convergence in Bayesian phylogenetics. fication. Biological Journal of the Linnean Society :–. Bioinformatics :–. Jones, A. W., and R. S. Kennedy. b. Plumage convergence and Oliveros, C. H., and R. G. Moyle. . Origin and diversifica- evolutionary history of the Island Thrush in the Philippines. Con- tion of Philippine bulbuls. Molecular Phylogenetics and Evolution dor :–. :–. Jønsson, K. A., R. C. K. Bowie, R. G. Moyle, L. Christidis, C. E. Peters, J. L. . Check-list of Birds of the World, vol. . Harvard Filardi, J. A. Norman, and J. Fjeldså. . Molecular phylo- University Press, Cambridge, Massachusetts. genetics and diversification within one of the most geographically Peterson, A. T. . Geographic variation in size and coloration in variable bird species complexes Pachycephala pectoralis/melan- the Turdus poliocephalus complex: A first review of species limits. ura. Journal of Avian Biology :–. Scientific Papers, Natural History Museum, University of Kansas Kennedy, R. S., P. C. Gonzales, E. C. Dickinson, H. C. :–. Miranda, Jr., and T. H. Fisher. . A Guide to the Birds of Pulvers, J. N., and D. J. Colgan. . Molecular phylogeography the Philippines. Oxford University Press, New York. of the fruit bat genus Melonycteris in northern Melanesia. Journal Kimball, R. T., E. L. Braun, F. K. Barker, R. C. K. Bowie, M. J. of Biogeography :–. Braun, J. L. Chojnowski, S. J. Hackett, K.-L. Han, J. Harsh- Rambaut, A., and A. J. Drummond. . TRACER, version .. man, V. Heimer-Torres, and others. . A well-tested set Available at beast.bio.ed.ac.uk/Tracer. of primers to amplify regions spread across the avian genome. Ronquist, F., and J. P. Huelsenbeck. . MrBayes: Bayes- Molecular Phylogenetics and Evolution :–. ian phylogenetic inference under mixed models. Bioinformatics Lim, H. C., F. H. Sheldon, and R. G. Moyle. . Extensive color :–. polymorphism in the Southeast Asian Oriental Dwarf Kingfisher Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, Ceyx erithaca: A result of gene flow during population diver- A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard, gence? Journal of Avian Biology :–. and J. P. Huelsenbeck. . MRBAYES .: Efficient Bayesian JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —129

phylogenetic inference and model choice across a large model Sukumaran, J., and M. T. Holder. . DendroPy. A Python space. Systematic Biology :–. library for phylogenetic computing. Bioinformatics : Roulin, A. . The evolution, maintenance and adaptive func- –. tion of genetic colour polymorphism in birds. Biological Reviews Theron, E., K. Hawkins, E. Bermingham, R. E. Ricklefs, and :–. N. I. Mundy. . The molecular basis of avian plumage poly- Sánchez-González, L. A., and R. G. Moyle. . Molec- morphism in the wild: A melanocortin--receptor point mutation ular systematics and species limits in the Philippine fantails is perfectly associated with the melanic plumage morph of the (Aves: Rhipidura). Molecular Phylogenetics and Evolution : bananaquit, Coereba flaveola. Current Biology :–. –. Uy, J. A. C., R. G. Moyle, and C. E. Filardi. a. Plumage Sheldon, F. H., C. H. Oliveros, S. S. Taylor, B. McKay, H. C. and song differences mediate species recognition between Lim, M. A. Rahman, H. Mays, and R. G. Moyle. . Molec- incipient flycatcher species of the Solomon Islands. Evolution ular phylogeny and insular biogeography of the lowland tailor- :–. birds of Southeast Asia (Cisticolidae: Orthotomus). Molecular Uy, J. A. C., R. G. Moyle, C. E. Filardi, and Z. A. Cheviron. b. Phylogenetics and Evolution :–. Difference in plumage color used in species recognition between Shimodaira, H. . An approximately unbiased test of phyloge- incipient species is linked to a single amino acid substitution in the netic tree selection. Systematic Biology :–. melanocortin- receptor. American Naturalist :–. Shimodaira, H., and M. Hasegawa. . CONSEL: For assess- Wiley, E. O. . The evolutionary species concept reconsidered. ing the confidence of phylogenetic tree selection. Bioinformatics Systematic Biology :–. :–. Wilgenbusch, J. C., D. L. Warren, and D. L. Swofford. . AWTY: Siler, C. D., J. R. Oaks, J. A. Esselstyn, A. C. Diesmos, and R. M. A system for graphical exploration of MCMC convergence in Bayesian Brown. . Phylogeny and biogeography of Philippine bent- phylogenetic inference. [Online.] Available at ceb.csit.fsu.edu/awty. toed geckos (Gekkonidae: Cyrtodactylus) contradict a prevailing Woodall, P. F. . Family Alcedinidae (Kingfishers). Pages – model of Pleistocene diversification. Molecular Phylogenetics and  in Handbook of the Birds of the World, vol. : Mousebirds to Evolution :–. Hornbills (J. del Hoyo, A. Elliott, and J. Sargatal, Eds.). Lynx Edi- Simpson, G. G. . Principles of Animal Taxonomy. Columbia cions, Barcelona, Spain. University Press, New York. Zwickl, D. J. . Genetic algorithm approaches for the phylo- Smith, C. E., and C. E. Filardi. . Patterns of molecular and genetic analysis of large biological sequence datasets under the morphological variation in some Solomon Island land birds. Auk maximum likelihood criterion. Ph.D. dissertation, University of :–. Texas, Austin. Sorenson, M. D., and T. W. Quinn. . Numts: A challenge for avian systematics and population biology. Auk :–. Associate Editor: L. Joseph 130 — ANDERSEN ET AL. — AUK, VOL. 130 ) feet Red Orange Orange Legs and continued ( belly yellow orange orange, orange, belly pale pale belly Breast and and Breast Breast rich rich Breast Breast dark dark Breast rich orange rich Rich orangeRich Orange Rich orangeRich Orange Rich orangeRich Orange rufous, belly rufous, belly white white white white white Male: Male: throat White Yellow- White White Orange white; female: Chin and Chin yellowish- Yellowish- Yellowish- Yellowish- Yellowish- Brilliant Brilliant Brilliant rine blue rine silvery-blue purple-blue purple-blue Brilliant dark morph: ultrama- ultramarine-blue ultramarine-blue cobalt blue; dark blue; dark cobalt Pale morph: pale ultramarine–blue blue Brilliant Brilliant Brilliant pale silvery silvery pale ultramarine ultramarine silvery-blue silvery-blue purple-blue purple-blue Silvery-blue Brilliant cobalt blue; cobalt Silvery-blue Brilliant Pale morph: dark morph: Brilliant pale Brilliant blue; dark pale cobalt cobalt pale silvery-blue silvery-blue purple-blue purple-blue marine blue marine-blue marine-blue morph: ultra- Brilliant ultra- Neck Neck blaze Back Rump Uppertail coverts White pale Brilliant black stripe Malar Malar Orange morph: Pale , based on examination of specimens at the University of Kansas Institute the (1992). and from Biodiversity of specimens Fry at University et, based al. on examination Dark Male: Male: White White Brilliant ultra- orange Yellow- Orange Brilliant Orange Blue- Orange Brilliant orange; chestnut and small and small female: lore of eye black of eye area in front front in area Ceyx lepidus Ceyx blue blue rine blue rine dark blue dark blue ultramarine Black, spottedBlack, Blackish, almost morph: ultrama- cobalt blue; dark blue; dark cobalt Pale morph: pale and washed with spotted with very spotted with very spotted with dark spotted with dark without dark blue dark without Black, washed and Black, washed and Black, washed and Black, washed and blue blue blue dark blue; and spotted and spotted and spotted and spotted washed and stripe on the the on stripe spotted with without dark dark without of neck blaze restricted to a with very dark with very dark with dark blue with dark blue Black, washed Black, washed tramarine blue tramarine an area front in hindcrown and hindcrown with blue-black dark morph: ul- Female: orange, Blackish, almost pale cobalt blue; blue; cobalt pale Red Male: black, Red Black, washed Red morph: Pale dible dible man- man- Black Black, washed lower black, Upper yellow mainly stouter stouter Red but Red Red but Red Phenotypic characters of the 15 subspecies of subspecies Phenotypic of the characters 15 . collectoris malaitae gentianus rethae PPENDIX C. l. dispar l. C. Subspecies Bill Head Wings spot Frontal A C. l. cajeli C. l. C. l. l. C. C. l. l. C. C. l. lepidus C. l. C. l. l. C. C. l. marga- l. C. JANUARY 2013 — CEYX LEPIDUS PHYLOGEOGRAPHY —131 feet pink Flesh- Yellow Orange Orange Legs and belly yellow yellow female orange orange, orange, orange- undertail belly and belly Dark rich yellow on Breast and and Breast Breast rich rich Breast ish-buff on male, moremale, Rich orangeRich Orange Rich orangeRich Orange Rich orangeRich Orange Rich orangeRich Orange Pale yellow- coverts very pale orange- pale white white white white white throat female orange- Chin and Chin ish-white yellow on Yellowish- Yellowish- Yellowish- Yellowish- ish-buff on male, moremale, Rich yellow- Rich Brilliant Brilliant Brilliant Cobalt blue Pale yellow Pale orange- purple-blue ultramarine-blue ultramarine-blue ultramarine-blue ultramarine-blue Ultramarine-blue Yellowish- Silvery blue Pale yellow- Pale Brilliant cobalt-blue purple-blue Silvery-blue Brilliant Silvery-blue Brilliant marine-blue marine-blue marine-blue Brilliant pale Brilliant ultra- Brilliant ultra- Brilliant ultra- pale blue pale cobalt-blue purple-blue marine-blue marine-blue marine-blue marine-blue marine-blue Brilliant ultra- Brilliant ultra- Lower mantle buff pale pale pale pale Neck Neck blaze Back Rump Uppertail coverts Male: Male: lowish yellow yellow- orange- Female: ish-buff; Pale yel- Pale stripe Malar Malar white female Orange ultra- Brilliant Orange Brilliant Orange pale Brilliant Orange ultra- Brilliant Orange ultra- Brilliant ish-buff orange- yellow on Yellowish- ish-buff on male, moremale, Pale yellow- Pale yellow- blue blue blue (paler) dark blue Black, softly tramarine blue spotted with very gled with pale ul- spotted with blue spotted with dark spotted with dark spotted with dark Blue-black, span- Blue-black, span- washed and spot- ted with dark blue Black, washed and Black, washed and Black, washed and Black, washed and Black, washed and gled with pale blue blue blue pale blue pale dark blue and spotted and spotted and spotted and spotted and spotted washed and Black, softly spotted with spangled with spangled with with very dark with dark blue with dark blue with dark blue Black, washed Black, washed with blue (paler)with blue pale ultramarine ultramarine pale red Red Black, washed red, red, Red, dible dible dible man- man- man- more more Black Black, washed Black Blue-black, Black Blue-black, Black Black, washed lower lower dusky black, Upper Upper mainly mainly ble redble mandi- slender orange- Continued. . maxilla mulcatus sacerdotis solitarius gialis PPENDIX Subspecies Bill Head Wings spot Frontal A C. l. meeki l. C. nigro- l. C. C. l. l. C. C. l. pallidus l. C. C. l. wallacii l. C. C. l. l. C. C. l. l. C. uropy- l. C.