Abstract
The Philippine archipelago is recognized as a biodiversity hotspot because of its high levels of endemism and numerous threatened species. Avian lineages in the Philippines feature morphologically distinct allopatric taxa, which have been variably treated either as species or subspecies depending on species concepts and recognition criteria. To understand how alternative species limits would alter diversity metrics and patterns of endemism in the Philippines, we selected 19 focal lineages of birds, each containing multiple described taxa within the Mindanao Island Group. We delimited species in an integrative, lineage-based framework using three operational criteria: species must (1) form well-supported, geographically circumscribed clades, (2) be monophyletic with significant genetic differentiation identified by a coalescent model, and (3) feature fixed differences in phenotypic characters. Our criteria identified 40 species from the original 19 focal lineages, a 50–74% increase over recent comprehensive taxonomic treatments. Genetic criteria in isolation identified an additional 10 populations that could be cryptic species in need of further study. We identified fine-scale endemism within the Mindanao Island Group, with multiple unrecognized avian endemics restricted to Samar/Leyte, Bohol Island, and the Zamboanga Peninsula. Genetic and phenotypic information support the hypothesis that polytypic bird species in the Philippines tend to be composed of evolutionarily distinct, range-restricted, allopatric replacements rather than widespread and variable “superspecies”. We conclude that lack of species recognition has resulted in underestimates of species diversity and overlooked fine-scale endemism in the Philippines. Recognizing this diversity would alter conservation priorities, shifting efforts to protect microendemics on smaller islands and finer scale endemic areas within larger islands.
This is a preview of subscription content, access via your institution.




Data accessibility
All DNA sequences generated for this project are archived on GenBank (MH379402-MH379451, MH384612-MH384765). Detailed sampling table (Online Appendix 1), Nexus-formatted alignments (Online Appendix 2), detailed phylogenetic trees (Online Appendix 3), and bGMYC output plots (Online Appendix 4), for each focal lineage are archived on Peter Hosner’s FigShare page at https://doi.org/10.6084/m9.figshare.6349415.
References
Andersen MJ, Nyári ÁS, Mason I et al (2013a) Molecular systematics of the world's most polytypic bird: the Pachycephala pectoralis/ melanura (Aves: Pachycephalidae) species complex. Zool J Linn Soc 170:566–588. https://doi.org/10.1111/zoj.12088
Andersen MJ, Oliveros CH, Filardi CE, Moyle RG (2013b) Phylogeography of the Variable Dwarf-Kingfisher Ceyx lepidus (Aves: Alcedinidae) inferred from mitochondrial and nuclear DNA sequences. Auk 130:118–131. https://doi.org/10.1525/auk.2012.12102
Andersen MJ, Shult HT, Cibois A et al (2015) Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus). R Soc Open Sci 2:140375–140375. https://doi.org/10.1073/pnas.1405000111
Andersen MJ, Manthey JD, Naikatini A, Moyle RG (2017) Conservation genomics of the silktail (Aves: Lamprolia victoriae) suggests the need for increased protection of native forest on the Natewa Peninsula, Fiji. Conserv Genet 18:1277–1285. https://doi.org/10.1007/s10592-017-0979-x
Barrowclough GF, Cracraft J, Klicka J, Zink RM (2016) How many kinds of birds are there and why does it matter? PLoS ONE 11:e0166307. https://doi.org/10.1371/journal.pone.0166307.s004
Brown RM, Diesmos AC (2002) Application of lineage-based species concepts to oceanic island frog populations: the effects of differing taxonomic philosophies on the estimation of Philippine biodiversity. Silliman J 42:133–162
Brown RM, Siler CD, Oliveros CH et al (2013) Evolutionary processes of diversification in a model island archipelago. Ann Rev Ecol Syst 44:24.1–24.25. https://doi.org/10.1146/annurev-ecolsys-110411-160323
Brown RM, Weghorst JA, Olson KV et al (2014) Conservation genetics of the Philippine tarsier: Cryptic genetic variation restructures conservation priorities for an island Archipelago primate. PLoS ONE 9:e104340–e104310. https://doi.org/10.1371/journal.pone.0104340
Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383
Collar NJ (2007) Philippine bird taxonomy and conservation: a commentary on Peterson (2006). Bird Conserv Int 17:103–113
Collar NJ (2011) Species limits in some Philippine birds including the greater flameback Chrysocolaptes lucidus. Forktail 27:29–38
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Incorporated, Sunderland, MA
Cracraft J (1983) Species concepts and speciation analysis. In: Current ornithology. Springer, Boston, MA, pp 159–187
Dayrat B (2005) Towards integrative taxonomy. Biol J Lin Soc 85:407–415
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886
Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340
del Hoyo J, Collar NJ (2014) HBW and birdlife international illustrated checklist of the birds of the world. Lynx Communications, Barcelona
del Hoyo J, collar NJ (2017) HBW and birdlife international illustrated checklist of the birds of the world. Lynx Ediciones, Barcelona
Delacour J, Mayr E (1945) Notes on the taxonomy of the birds of the Philippines. Zoologica 30:105–117
Dickerson RE, Merrill ED, McGregor RC et al (1928) Distribution of life in the Philippines. Bureau of Printing, Manila
Drovetski S, Zink RM, Fadeev IV et al (2004) Mitochondrial phylogeny of Locustella and related genera. J Avian Biol 35:105–110
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
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. https://doi.org/10.1644/07-MAMM-A-285.1
Fujita MK, Leaché AD, Burbrink FT et al (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27:480–488. https://doi.org/10.1016/j.tree.2012.04.012
Gill FB (2014) Species taxonomy of birds: which null hypothesis? Auk 131:150–161. https://doi.org/10.1642/AUK-13-206.1
Gill F, Donsker D (2017) IOC world bird names (version 7.3)
Hackett S (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Mol Phylogen Evol 5:368–382
Heaney LR (1985) Zoogeographic evidence for middle and late Pleistocene land bridges to the Philippine Islands. Mod Quat Res Southeast Asia 9:127–144
Heaney LR (1986) Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biol J Lin Soc 28:127–165
Heaney LR, Balete DS, Duya MR et al (2016) Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island. Front Biogeogr 8.2:1–19
Ho SYW, Duchêne S (2014) Molecular-clock methods for estimating evolutionary rates and timescales. Mol Ecol 23:5947–5965. https://doi.org/10.1111/mec.12953
Hosner PA, Sheldon FH, Lim HC, Moyle RG (2010) Phylogeny and biogeography of the Asian trogons (Aves: Trogoniformes) inferred from nuclear and mitochondrial DNA sequences. Mol Phylogen Evol 57:1219–1225. https://doi.org/10.1016/j.ympev.2010.09.008
Hosner PA, Boggess NC, Alviola P et al (2013a) Phylogeography of the Robsonius ground-warblers (Passeriformes: Locustellidae) reveals an undescribed species from northeastern Luzon, Philippines. The Condor 115:630–639. https://doi.org/10.1525/cond.2013.120124
Hosner PA, Nyári ÁS, Moyle RG (2013b) Water barriers and intra-island isolation contribute to diversification in the insular Aethopyga sunbirds (Aves: Nectariniidae). J Biogeogr 64:1094–1106. https://doi.org/10.1111/jbi.12074
Hosner PA, Sánchez-González LA, Peterson AT, Moyle RG (2014) Climate-driven diversification and Pleistocene refugia in Philippine birds: evidence from phylogeographic structure and paleoenvironmental niche modeling. Evolution 68:2658–2674. https://doi.org/10.1111/evo.12459
Irestedt M, Fabre PH, Batalha-Filho H et al (2013) The spatio-temporal colonization and diversification across the Indo-Pacific by a “great speciator” (Aves, Erythropitta erythrogaster). Proc R Soc B 280:20130309–20130309. https://doi.org/10.1371/journal.pone.0004379
Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383–2394
Isler ML, Isler PR, Whitney BM (1998) Use of vocalizations to establish species limits in antbirds (Passeriformes: Thamnophilidae). Auk 115:577–590
Jones A, Kennedy R (2008) Evolution in a tropical archipelago: comparative phylogeography of Philippine fauna and flora reveals complex patterns of colonization and diversification. Biol J Lin Soc 95:620–639
Jønsson KA, Bowie R, Moyle R et al (2008) Molecular phylogenetics and diversification within one of the most geographically variable bird species complexes Pachycephala pectoralis/melanura. J Avian Biol 39:473–478
Kearns AM, Restani M, Szabo I et al (2018) Genomic evidence of speciation reversal in ravens. Nat Commun. https://doi.org/10.1038/s41467-018-03294-w
Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kennedy RS, Gonzales PC, Dickinson EC (2000) A guide to the birds of the Philippines. Oxford University Press, New York
Lohman DJ, Ingram KK, Prawiradilaga DM et al (2010) Cryptic genetic diversity in “widespread” Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biol Conserv 143:1885–1890. https://doi.org/10.1016/j.biocon.2010.04.042
Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc B 359:711–719. https://doi.org/10.1098/rstb.2003.1454
Maddison W (1997) Gene trees in species trees. Syst Biol 46:523
Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Columbia University Press, New York, NY
Mayr E, Amadon D (1951) A classification of recent birds. Am Mus Novit 1496:1–42
McCormack JE, Hird SM, Zellmer AJ et al (2013) Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogen Evol 66:526–538. https://doi.org/10.1016/j.ympev.2011.12.007
McGregor RC (1909) A manual of Philippine birds. Bureau of Printing, Manila
Mckay BD, Zink RM (2010) The causes of mitochondrial DNA gene tree paraphyly in birds. Mol Phylogen Evol 54:647–650. https://doi.org/10.1016/j.ympev.2009.08.024
McKitrick MC, Zink RM (1988) Species concepts in ornithology. Condor 90:1–14. https://doi.org/10.2307/1368426
Miller KG (2005) The phanerozoic record of global sea-level change. Science 310:1293–1298. https://doi.org/10.1126/science.1116412
Miranda HC Jr, Brooks DM, Kennedy RS (2011) Phylogeny and taxonomic review of Philippine lowland scops owls (Strigiformes): parallel diversification of highland and lowland clades. Wilson J 123:441–453
Moltesen M, Irestedt M, Fjeldså J et al (2012) Molecular phylogeny of Chloropseidae and Irenidae: cryptic species and biogeography. Mol Phylogenet Evol 65:903–914. https://doi.org/10.1016/j.ympev.2012.08.012
Moritz C, Cicero C (2004) DNA barcoding: promise and pitfalls. PLoS Biol 2:e279–e354
Moyle RG, Andersen MJ, Oliveros CH et al (2012) Phylogeny and biogeography of the core babblers (Aves: Timaliidae). Syst Biol 61:631–651. https://doi.org/10.1093/sysbio/sys027
Moyle RG, Manthey JD, Hosner PA et al (2017) A genome-wide assessment of stages of elevational parapatry in Bornean passerine birds reveals no introgression: implications for processes and patterns of speciation. PeerJ 5:e3335–e3318. https://doi.org/10.7717/peerj.3335
Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Navarro-Sigüenza AG, Peterson AT (2004) An alternative species taxonomy of the birds of Mexico. Biota Neotrop 4:BN03504022004
Nyári ÁS, Peterson AT, Rice NH, Moyle RG (2009) Phylogenetic relationships of flowerpeckers (Aves: Dicaeidae): novel insights into the evolution of a tropical passerine clade. Mol Phylogen Evol 53:613–619. https://doi.org/10.1016/j.ympev.2009.06.014
Oliveros CH, Moyle RG (2010) Origin and diversification of Philippine bulbuls. Mol Phylogen Evol 54:822–832. https://doi.org/10.1016/j.ympev.2009.12.001
Orme CDL, Davies RG, Burgess M et al (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019. https://doi.org/10.1038/nature03850
Padial J, Miralles A, la Riva De I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16
Paguntalan L, Jakosalem PG (2008) Significant records of birds in forests on Cebu island, central Philippines. Forktail 24:48–56
Peterson AT (2006) Taxonomy is important in conservation: a preliminary reassessment of Philippine species-level bird taxonomy. Bird Conserv Int 16:155–173
Peterson AT, Navarro-Sigüenza AG (1999) Alternate species concepts as bases for determining priority conservation areas. Conserv Biol 13:427–431. https://doi.org/10.1046/j.1523-1739.1999.013002427.x
Peterson AT, Ball LG, Brady KW (2000) Distribution of the birds of the Philippines: biogeography and conservation priorities. Bird Conserv Int 10:149–167
Pons J, Barraclough T, Gomez-Zurita J et al (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609. https://doi.org/10.1080/10635150600852011
Posa MRC, Diesmos AC, Sodhi NS, Brooks TM (2008) Hope for threatened tropical biodiversity: lessons from the Philippines. Bioscience 58:231–240. https://doi.org/10.1641/B580309
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Pratt HD (2010) Revisiting species and subspecies of island birds for a better assessment of biodiversity. Ornithol Monogr 67:78–89. https://doi.org/10.1525/om.2010.67.1.79
Price T (2008) Speciation in birds. Roberts & Company, Greenwood Village, Colorado.
Rambaut A, Drummond AJ (2007) Tracer version 1.5. Available at http://tree.bio.ed.ac.uk/software/tracer/
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 12:1–1. https://doi.org/10.1186/1471-2148-12-196
Sánchez-González LA, Moyle RG (2011) Molecular systematics and species limits in the Philippine fantails (Aves: Rhipidura). Mol Phylogen Evol 61:290–299. https://doi.org/10.1016/j.ympev.2011.06.013
Sánchez-González LA, Hosner PA, Moyle RG (2015) Genetic differentiation in insular lowland rainforests: insights from historical demographic patterns in Philippine Birds. PLoS ONE 10:e0134284. https://doi.org/10.1371/journal.pone.0134284.s002
Sangster G (2000) Taxonomic stability and avian extinctions. Conserv Biol 14:579–581
Sangster G (2009) Increasing numbers of bird species result from taxonomic progress, not taxonomic inflation. Proc R Soc B 276:3185–3191. https://doi.org/10.1126/science.1122806
Sangster G, King BF, Verbelen P, Trainor CR (2013) A new owl species of the genus Otus (Aves: Strigidae) from Lombok, Indonesia. PLoS ONE 8:e53712. https://doi.org/10.1371/journal.pone.0053712
Sanguila MB, Siler CD, Diesmos AC et al (2011) Phylogeography, geographic structure, genetic variation, and potential species boundaries in Philippine slender toads. Mol Phylogen Evol 61:333–350. https://doi.org/10.1016/j.ympev.2011.06.019
Sheldon FH, Oliveros CH, Taylor SS et al (2012) Molecular phylogeny and insular biogeography of the lowland tailorbirds of Southeast Asia (Cisticolidae: Orthotomus). Mol Phylogen Evol 65:54–63. https://doi.org/10.1016/j.ympev.2012.05.023
Siddall M, Rohling E, Almogi-Labin A et al (2003) Sea-level fluctuations during the last glacial cycle. Nature 423:853–858
Siler CD, Oaks JR, Esselstyn JA et al (2010) Phylogeny and biogeography of Philippine bent-toed geckos (Gekkonidae: Cyrtodactylus) contradict a prevailing model of Pleistocene diversification. Mol Phylogen Evol 55:699–710. https://doi.org/10.1016/j.ympev.2010.01.027
Simpson GG (1951) The species concept. Evolution 5:285. https://doi.org/10.2307/2405675
Smith BT, Ribas CC, Whitney BM et al (2013) Identifying biases at different spatial and temporal scales of diversification: a case study in the Neotropical parrotlet genus Forpus. Mol Ecol 22:483–494. https://doi.org/10.1111/mec.12118
Sorenson M, Ast J, Dimcheff D et al (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogen Evol 12:105–114
Stattersfield AJ, Crosby MJ, Long AJ (1998) Endemic bird areas of the world. BirdLife International, Cambridge U.K
Tobias JA, Seddon N, Spottiswoode CN et al (2010) Quantitative criteria for species delimitation. Ibis 152:724–746. https://doi.org/10.1111/j.1474-919X.2010.01051.x
Voris H (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167
Watson DM (2005) Diagnosable versus distinct: evaluating species limits in birds. Bioscience 55:60–68
Welton LJ, Siler CD, Grismer LL et al (2016) Archipelago-wide survey of Philippine forest dragons (Agamidae: Gonocephalus): multilocus phylogeny uncovers unprecedented levels of genetic diversity in a biodiversity hotspot. Biol J Lin Soc. https://doi.org/10.1111/bij.12878
Wiens JJ, Servedio MR (2000) Species delimitation in systematics: inferring diagnostic differences between species. Proc R Soc Lond B: Biol Sci 267:631–636
Wiley EO (1978) The evolutionary species concept reconsidered. Syst Biol 27:17–26
Will K, Mishler B, Wheeler Q (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54:844–851. https://doi.org/10.1080/10635150500354878
Wood SD, Schnell GD (1986) Revised world inventory of avian skeletal specimens. American Ornithologists’ Union and Oklahoma Biological Survey, Washington, DC
Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc B 271:561–564. https://doi.org/10.1098/rspb.2003.2617
Acknowledgements
We would like to thank field collectors who contributed genetic samples and specimens to this project. Several museums supplied tissue grants: The American Museum of Natural History (Paul Sweet), Cincinnati Museum of Natural History (Herman Mays), Field Museum of Natural History (Dave Willard), Louisiana State Museum of Natural Science (Donna Dittman and Steve Cardiff) and the University of Kansas Biodiversity Institute (Mark Robbins). The National Science Foundation (DEB-0743491 and DEB-1241181), American Ornithologists’ Union, American Museum of Natural History Chapman Fund, and the University of Kansas Panorama Fund supported fieldwork, The National Science Foundation (DEB-1110619) and the University of Kansas Graduate Student Research Fund supported lab work. Consejo Nacional de Ciencia y Tecnología (CONACyT) funded a postdoctoral fellowship (Expediente 93730) to LASG at the University of Kansas. We are grateful to the Department of Environment and Natural Resources and the Protected Areas and Wildlife Bureau of the Philippines for facilitating collecting and export permits. Joe Manthey, Hannah Owens, and Town Peterson gave helpful comments that improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hosner, P.A., Campillo, L.C., Andersen, M.J. et al. An integrative species delimitation approach reveals fine-scale endemism and substantial unrecognized avian diversity in the Philippine Archipelago. Conserv Genet 19, 1153–1168 (2018). https://doi.org/10.1007/s10592-018-1085-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-018-1085-4