Advertisement

Journal of Ornithology

, Volume 160, Issue 1, pp 1–16 | Cite as

Molecular evidence suggests radical revision of species limits in the great speciator white-eye genus Zosterops

  • Bryan T. M. Lim
  • Keren R. Sadanandan
  • Caroline Dingle
  • Yu Yan Leung
  • Dewi M. Prawiradilaga
  • Mohammad Irham
  • Hidayat Ashari
  • Jessica G. H. Lee
  • Frank E. RheindtEmail author
Original Article

Abstract

White-eyes (Zosterops spp.) are a group of small passerines distributed across the Eastern Hemisphere that have become a textbook example of rapid speciation. However, traditional taxonomy has relied heavily on conservative plumage features to delimit white-eye species boundaries, resulting in several recent demonstrations of misclassification. Resolution of confused taxonomy is important in order to correctly delimit species and identify taxa which may require conservation, particularly in Asia where the songbird trade is decimating wild populations. In this study, we aim to untangle multiple instances of confused taxonomic treatment in three large, widespread Asian wastebasket species complexes of white-eye (Oriental White-eye Zosterops palpebrosus, Japanese White-eye Zosterops japonicus and Mountain White-eye Zosterops montanus) renowned for their conservative morphology. Using mitochondrial DNA from 173 individuals spanning 42 taxa, we uncovered extensive polyphyly in Z. palpebrosus and Z. japonicus and propose some radically revised species limits under which former members of Z. palpebrosus and Z. japonicus would be reassigned into four and two different species, respectively. The revised taxonomy results in a net loss of two previously recognized species and a net gain of two newly recognized species, leading to significant taxonomic change but a lack of additional species-level diversity. One of the newly elevated species, Zosterops melanurus from Java and Bali, is also the world’s most heavily traded songbird and requires urgent conservation attention.

Keywords

Cryptic speciation Phylogenetics Wastebasket species Polyphyly Taxonomy 

Zusammenfassung

Molekulare Belege erfordern eine radikale Revision der Artgrenzen innerhalb der „Superartbildner“-Brillenvogelgattung Zosterops

Brillenvögel (Zosterops spp.) sind eine Gruppe kleiner Singvögel der östlichen Hemisphäre, die zu einem Paradebeispiel für schnelle Artbildung geworden sind. Allerdings stützte sich die traditionelle Taxonomie bei der Abgrenzung der Brillenvogelarten bisher vorwiegend auf konservative Gefiedermerkmale, was zu verschiedenen in neuerer Zeit aufgedeckten Falschklassifikationen führte. Eine Entwirrung der Taxonomie ist wichtig für eine korrekte Artabgrenzung und die Ermittlung von Taxa mit besonderem Schutzbedarf, speziell in Asien, wo der Handel mit Singvögeln die Wildpopulationen stark dezimiert. Ziel dieser Untersuchung war es, verschiedene Fälle verworrener taxonomischer Einordnung bei drei großen, weitverbreiteten asiatischen “Sammelsurium-Artkomplexen” von Brillenvögeln (Gangesbrillenvogel Z. palpebrosus, Japanbrillenvogel Z. japonicus und Gebirgsbrillenvogel Z. montanus) aufzulösen, welche für ihre konservative Morphologie bekannt sind. Anhand von mitochondrialer DNA von 173 Individuen aus 42 Taxa entdeckten wir ein beträchtliches Maß an Polyphylie bei Z. palpebrosus sowie Z. japonicus und empfehlen eine radikale Revision einiger Artgrenzen, durch welche vormalige Angehörige der Arten Z. palpebrosus und Z. japonicus neu zu jeweils vier beziehungsweise zwei verschiedenen Arten gerechnet würden. Diese überarbeitete Taxonomie resultiert insgesamt in dem Verlust zweier vormals anerkannter Arten sowie einem Hinzugewinn von zwei neu etablierten Arten, was zwar zu einer signifikanten taxonomischen Veränderung, jedoch nicht zu zusätzlicher Diversität auf Artebene führt. Eine der neu anerkannten Arten, Z. melanurus von Java und Bali, ist zudem der meistgehandelte Singvogel der Welt und bedarf dringender Schutzmaßnahmen.

Notes

Acknowledgements

We thank C. Y. Gwee, N. S. R. Ng, E. Y. X. Ng, Q. Tang, G. W. J. Low, P. Baveja, J. Y. Lim, H. Z. Tan, D. Y. J. Ng, R. Y. C. Teo, Y. F. Chung, J. E. H. Ang, A. Y. H. Tan and J. S. M. Soh for field support, lab support and/or valuable feedback on this manuscript. We acknowledge grants from Wildlife Reserves Singapore (R-154-000-A05-592) and Wildlife Reserves Singapore Conservation Fund (R-154-000-A99-592) for funding this project. We are indebted to Wildlife Reserves Singapore, the Lee Kong Chian Natural History Museum (Singapore), the Burke Museum of Natural History and Culture (Seattle, WA), Museum Zoologicum Bogoriense (Cibinong, West Java, Indonesia) and the Hong Kong Bird Watching Society Ringing Team for providing samples for this study. The National Parks Board of Singapore is acknowledged for facilitating fieldwork. The experiments comply with the laws of the Republic of Singapore and Hong Kong.

Supplementary material

10336_2018_1583_MOESM1_ESM.pdf (270 kb)
Supplementary material 1 (PDF 270 kb)

References

  1. BirdLife International (2018) Zosterops flavus. http://www.birdlife.org. Accessed 24 Jan 2018
  2. Chng SCL, Eaton JA (2016) In the market for extinction: eastern and central Java. TRAFFIC report, Petaling JayaGoogle Scholar
  3. Chng SCL, Eaton JA, Krishnasamy K, Shepherd CR, Nijman V (2015) In the market for extinction: an inventory of Jakarta’s bird markets. TRAFFIC report, Petaling JayaGoogle Scholar
  4. Cibois A, Pasquet E, Schulenberg TS (1999) Molecular systematics of the Malagasy babblers (Passeriformes: Timaliidae) and warblers (Passeriformes: Sylviidae), based on cytochrome b and 16S rRNA sequences. Mol Phylogenetics Evol 13(3):581–595CrossRefGoogle Scholar
  5. Cornetti L, Valente LM, Dunning LT, Quan X, Black RA, Hébert O, Savolainen V (2015) The genome of the “great speciator” provides insights into bird diversification. Genome Biol Evol 7:2680–2691CrossRefGoogle Scholar
  6. Cox SC, Prys-Jones RP, Habel JC, Amakobe BA, Day JJ (2014) Niche divergence promotes rapid diversification of East African sky island white-eyes (Aves: Zosteropidae). Mol Ecol 23(16):4103–4118CrossRefGoogle Scholar
  7. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  8. 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 73:2160–2164CrossRefGoogle Scholar
  9. Dong F, Li SH, Yang XJ (2010) Molecular systematics and diversification of the Asian scimitar babblers (Timaliidae, Aves) based on mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 57:1268–1275CrossRefGoogle Scholar
  10. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973CrossRefGoogle Scholar
  11. Eaton JA, Shepherd CR, Rheindt FE, Harris JBC, van Balen B, Wilcove D, Collar NJ (2015) Trade-driven extinctions and near-extinctions of avian taxa in Sundaic Indonesia. Forktail 31:1–12Google Scholar
  12. Eaton JA, van Balen B, Brickle NW, Rheindt FE (2016) Birds of the Indonesian Archipelago: Greater Sundas and Wallacea. Lynx, BarcelonaGoogle Scholar
  13. Eaton JA, Leupen BTC, Krishnasamy K (2017) Songsters of Singapore: an overview of the bird species in Singapore pet shops. TRAFFIC report, Petaling JayaGoogle Scholar
  14. Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253(4):769–778CrossRefGoogle Scholar
  15. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704CrossRefGoogle Scholar
  16. Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:16–174Google Scholar
  17. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, Suh A, Weber CC, da Fonseca RR, Li J, Zhang F, Li H, Zhou L, Narula N, Liu L, Ganapathy G, Boussau B, Bayzid MS, Zavidovych V, Subramanian S, Gabaldón T, Capella-Gutiérrez S, Huerta-Cepas J, Rekepalli B, Munch K, Schierup M, Lindow B, Warren WC, Ray D, Green RE, Bruford M, Zhan X, Dixon A, Li S, Li N, Huang Y, Derryberry EP, Bertelsen MF, Sheldon FH, Brumfield RT, Mello CV, Lovell PV, Wirthlin M, Cruz-Schneider MP, Prosdocimi F, Samaniego JA, Vargas-Velazquez AM, Alfaro-Núñez A, Campos PF, Petersen B, Sicheritz-Ponten T, Pas A, Bailey T, Scofield P, Bunce M, Lambert DM, Zhou Q, Perelman P, Driskell AC, Shapiro B, Xiong Z, Zeng Y, Liu S, Li Z, Liu B, Wu K, Xiao J, Yinqi X, Zheng Q, Zhang Y, Yang H, Wang J, Smeds L, Rheindt FE, Braun M, Fjeldså J, Orlando L, Barker K, Jønsson KA, Johnson W, Koepfli K-P, O’Brien S, Haussler D, Ryder OA, Rahbek C, Willerslev E, Graves GR, Glenn TC, McCormack J, Burt D, Ellegren H, Alström P, Edwards SV, Stamatakis A, Mindell DP, Cracraft J, Braun EL, Warnow T, Jun W, Gilbert MTP, Zhang G (2014) Whole genome analyses resolve early branches in the tree of life of modern birds. Science 346(6215):1320–1331CrossRefGoogle Scholar
  18. Jeyarajasingam A (2012) A field guide to the birds of Peninsular Malaysia and Singapore. Oxford University Press, OxfordGoogle Scholar
  19. Jones AW, Kennedy RS (2008) Evolution in a tropical archipelago: comparative phylogeography of Philippine fauna and flora reveals complex patterns of colonization and diversification. Biol J Linn Soc 95:620–639CrossRefGoogle Scholar
  20. Kanetsuki Y, Nagata H, Tsubaki Y (2006) Molecular analysis of the population genetics of the Japanese White-eye in Japan. J Ornithol 147(suppl):191Google Scholar
  21. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874CrossRefGoogle Scholar
  22. Lanfea R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29(6):1695–1701.  https://doi.org/10.1093/molbev/mss020 CrossRefGoogle Scholar
  23. Lee JGH, Chng SCL, Eaton JA (2016) Conservation strategy for Southeast Asian songbirds in trade. Recommendations from the first Asian Songbird Trade Crisis Summit 2015, Jurong Bird Park, Singapore, 27–29 Sep 2015Google Scholar
  24. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  25. Linck E, Schaack S, Dumbacher JP (2016) Genetic differentiation within a widespread “supertramp” taxon: molecular phylogenetics of the Louisiade White-eye (Zosterops griseotinctus). Mol Phylogenet Evol 94:113–121CrossRefGoogle Scholar
  26. Lovette IJ (2004) Mitochondrial dating and mixed support for the “2% rule” in birds. Auk 121(1):1–6Google Scholar
  27. Moyle RG, Filardi CE, Smith CE, Diamond J (2009) Explosive Pleistocene diversification and hemispheric expansion of a “great speciator”. Proc Natl Acad Sci 106:1863–1868CrossRefGoogle Scholar
  28. Nishiumi I, Kim CH (2004) Little genetic differences between Korean and Japanese populations in songbirds (Part two Natural History Studies). Natl Sci Mus Monogr 24:279–286Google Scholar
  29. Peterson AT (2006) Application of molecular clocks in ornithology revisited. J Avian Biol 37(6):541–544CrossRefGoogle Scholar
  30. Price TD, Hooper DM, Buchanan CD, Johansson US, Tietze DT, Alström P, Olsson U, Ghosh-Harihar M, Ishtiaq F, Gupta SK, Martens J, Harr B, Singh P, Mohan D (2014) Niche filling slows the diversification of Himalayan songbirds. Nature 509(7499):222–225CrossRefGoogle Scholar
  31. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526(7574):569CrossRefGoogle Scholar
  32. Rambaut A (2006) Tree figure drawing tool version 1.4.3. Institute of Evolutionary Biology, University of Edinburgh. https://tree.bio.ed.ac.uk/. Accessed July 2017
  33. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. https://tree.bio.ed.ac.uk/software/tracer/. Accessed July 2017
  34. Rasmussen PC, Anderton JC (2012) Birds of South Asia: the Ripley guide (2 vols, 2nd edn). Lynx, WashingtonGoogle Scholar
  35. Robson C (2005) Birds of Southeast Asia. New Holland, LondonGoogle Scholar
  36. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  37. Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12(2):105–114CrossRefGoogle Scholar
  38. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  39. Thompson JD, Gibson T, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 1:2–3Google Scholar
  40. van Balen B (2017a) White-eyes (Zosteropidae). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/52351on. Accessed 29 Mar 2017)
  41. van Balen B (2017b) Oriental White-eye (Zosterops palpebrosus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/60163on. Accessed 2 Apr 2017)
  42. van Balen B (2017c) Japanese White-eye (Zosterops japonicus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/60163on. Accessed 2 Apr 2017)
  43. van Balen B (2017d) Mountain White-eye (Zosterops montanus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds.) Handbook of the of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/60163on. Accessed 2 Apr 2017)
  44. van Balen B (2017e) Enggano White-eye (Zosterops salvadorii). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/60163on. Accessed 2 Apr 2017)
  45. van Balen B (2017f) Ashy-bellied White-eye (Zosterops citrinella). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from http://www.hbw.com/node/60163on. Accessed 2 Apr 2017)
  46. van Balen B (2018a) Mountain Black-eye (Chlorocharis emiliae). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from https://www.hbw.com/node/60251on. Accessed 23 Jan 2018)
  47. van Balen B (2018b) Everett’s White-eye (Zosterops everetti). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx, Barcelona. (retrieved from https://www.hbw.com/node/60171on. Accessed 22 May 2018)
  48. Warren BH, Bermingham E, Prys-Jones RP, Thebaud C (2006) Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands. Mol Ecol 15(12):3769–3786CrossRefGoogle Scholar
  49. Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17(10):2321–2328CrossRefGoogle Scholar
  50. Wells DR (2017a) Zosterops white-eyes in continental South-East Asia. 1. Proposed refinements to the regional definition of Oriental White-eye Z. palpebrosus. Bull Br Ornithol Club 137(2):100–109CrossRefGoogle Scholar
  51. Wells DR (2017b) Zosterops white-eyes in continental South-East Asia. 2. What is Zosterops auriventer Hume? Bull Br Ornithol Club 137(2):110–116CrossRefGoogle Scholar
  52. Wickramasinghe N, Robin VV, Ramakrishnan U, Reddy S, Seneviratne SS (2017) Non-sister Sri Lankan white-eyes (genus Zosterops) are a result of independent colonizations. PLoS One 12(8):e0181441CrossRefGoogle Scholar
  53. Woodruff DS (2010) Biogeography and conservation in Southeast Asia: how 2 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodivers Conserv 19(4):919–941CrossRefGoogle Scholar
  54. Yule GU (1925) A mathematical theory of evolution, based on the conclusions of Dr. JC Willis, FRS. Philos Trans R Soc B 213:21–87CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2018

Authors and Affiliations

  • Bryan T. M. Lim
    • 1
  • Keren R. Sadanandan
    • 1
  • Caroline Dingle
    • 2
  • Yu Yan Leung
    • 2
  • Dewi M. Prawiradilaga
    • 3
  • Mohammad Irham
    • 3
  • Hidayat Ashari
    • 3
  • Jessica G. H. Lee
    • 4
  • Frank E. Rheindt
    • 1
    Email author
  1. 1.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  2. 2.School of Biological Sciences, Kadoorie Biological Sciences BuildingUniversity of Hong KongHong Kong SARChina
  3. 3.Research Center for Biology-LIPICibinongIndonesia
  4. 4.Wildlife Reserves SingaporeSingaporeSingapore

Personalised recommendations