Journal of Ornithology

, Volume 156, Supplement 1, pp 325–331 | Cite as

Assessing the potential for reverse colonization among Japanese birds by mining DNA barcode data

  • Isao NishiumiEmail author
  • Chang-Hoe Kim


Reverse colonization from an island to a continent runs counter to the classic models of speciation in island biogeography. We mined the Barcode of Life Data Systems and generated mitochondrial DNA-based phylogenetic analyses for 118 Japanese bird species to identify candidates for reverse colonization histories from Japan to mainland Asia. Mitochondrial DNA tree topologies suggested 5 strong and 35 weak candidate species for reverse colonization from Japan to mainland Asia. Thirty-nine mitochondrial DNA topologies contradicted a reverse colonization hypothesis. For the remaining 39 species the ancestral distribution is ambiguous from the available mitochondrial DNA gene tree topology. A combination of geography and climatic and geologic history are likely drivers of avian speciation in the Japanese Islands and subsequent reverse colonization events to mainland Asia. These data highlight the utility of large scale DNA barcoding databases in generating phylogenetic and biogeographic hypotheses.


DNA barcode Island biogeography Japanese birds Reverse colonization Speciation 



We gratefully acknowledge logistic support and help by Drs. Alexey Kryukov, Yaroslav Red’kin, Irina Marova, Liudmila Spiridonova, Vladimir Ivanitskii, and every one of the staff at Moscow State University and at the Institute of Biology and Soil Science, Russian Academy of Sciences, Vladivostok. We thank an anonymous reviewer for many valuable comments that greatly improved our manuscript, and express special thanks to the contribution of Dr. Herman Mays Jr. that exceed the contribution as a reviewer. We also thank Drs. Takema Saitoh, Norimasa Sugita, and every Japanese ornithologist who conducted and supported DNA barcode of birds. We gratefully acknowledge financial support from JSPS KAKENHI Grant Number 24657066.

Supplementary material

10336_2015_1247_MOESM1_ESM.pdf (217 kb)
Supplementary Figure (PDF 216 kb)
10336_2015_1247_MOESM2_ESM.xlsx (23 kb)
Supplementary Table (XLSX 22 kb)


  1. Akimova A, Haring E, Kryukov S, Kryukov A (2007) First insights into a DNA sequence based phylogeny of the Eurasian jay Garrulus glandarius. Russ J Ornithol 16:567–575Google Scholar
  2. Bellemain E, Ricklefs RE (2008) Are islands the end of the colonization road? Trends Ecol Evol 23:461–468PubMedCrossRefGoogle Scholar
  3. Boedeker C, Eggert A, Immers A, Wakana I (2010) Biogeography of Aegagropila linnaei (Cladophorophyceae, Chlorophyta): a widespread freshwater alga with low effective dispersal potential shows a glacial imprint in its distribution. J Biogeogr 37:1491–1503Google Scholar
  4. Clare EL, Lim BK, Engstrom MD, Eger JL, Hebert PD (2007) DNA barcoding of neotropical bats: species identification and discovery within Guyana. Mol Ecol Notes 7:184–190CrossRefGoogle Scholar
  5. Clements JF (2007) Clements checklist of birds of the world. Christopher Helm, LondonGoogle Scholar
  6. Diamond JM (1977) Continental and insular speciation in Pacific land birds. Syst Biol 26:263–268CrossRefGoogle Scholar
  7. Dove CJ, Rotzel NC, Heacker M, Weigt LA (2008) Using DNA barcodes to identify bird species involved in birdstrikes. J Wildl Manag 72:1231–1236CrossRefGoogle Scholar
  8. Drovetski SV, Zink RM, Rohwer S, Fadeev IV, Nesterov EV, Karagodin I, Koblik EA, Red’kin YA (2004) Complex biogeographic history of a Holarctic passerine. Proc R Soc Lond B 271:545–551CrossRefGoogle Scholar
  9. Filardi CE, Moyle RG (2005) Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature 438:216–219PubMedCrossRefGoogle Scholar
  10. Haring E, Gamauf A, Kryukov A (2007) Phylogeographic patterns in widespread corvid birds. Mol Phylogenet Evol 45:840–862PubMedCrossRefGoogle Scholar
  11. Hebert PD, Cywinska A, Ball SL (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321CrossRefGoogle Scholar
  12. Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004a) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817PubMedPubMedCentralCrossRefGoogle Scholar
  13. Hebert PD, Stoeckle MY, Zemlak TS, Francis CM (2004b) Identification of birds through DNA barcodes. PLoS Biol 2:e312PubMedPubMedCentralCrossRefGoogle Scholar
  14. Hung CM, Drovetski SV, Zink RM (2012) Multilocus coalescence analyses support a mtDNA-based phylogeographic history for a widespread Palearctic passerine bird, Sitta europaea. Evolution 66:2850–2864PubMedCrossRefGoogle Scholar
  15. Johnsen A, Rindal E, Ericson PG, Zuccon D, Kerr KC, Stoeckle MY, Lifjeld JT (2010) DNA barcoding of Scandinavian birds reveals divergent lineages in trans-Atlantic species. J Ornithol 151:565–578CrossRefGoogle Scholar
  16. Jønsson KA, Fabre PH, Ricklefs RE, Fjeldså J (2011) Major global radiation of corvoid birds originated in the proto-Papuan archipelago. Proc Natl Acad Sci USA 108:2328–2333PubMedPubMedCentralCrossRefGoogle Scholar
  17. Kerr KC, Stoeckle MY, Dove CJ, Weigt LA, Francis CM, Hebert PD (2007) Comprehensive DNA barcode coverage of North American birds. Mol Ecol Notes 7:535–543PubMedPubMedCentralCrossRefGoogle Scholar
  18. Kerr KC, Lijtmaer DA, Barreira AS, Hebert PD, Tubaro PL (2009a) Probing evolutionary patterns in neotropical birds through DNA barcodes. PLoS ONE 4:e4379PubMedPubMedCentralCrossRefGoogle Scholar
  19. Kerr KC, Birks SM, Kalyakin MV, Red’kin YA, Koblik EA, Hebert PD (2009b) Filling the gap-COI barcode resolution in eastern Palearctic birds. Front Zool 6:29–42PubMedPubMedCentralCrossRefGoogle Scholar
  20. Lara A, Rodriguez R, Casane D, Cote G, Bernatchez L, Garcia-Machado E (2010) DNA barcoding of Cuban freshwater fishes: evidence for cryptic species and taxonomic conflicts. Mol Ecol Res 10:421–430CrossRefGoogle Scholar
  21. Lim HC, Sheldon FH (2011) Multilocus analysis of the evolutionary dynamics of rainforest bird populations in Southeast Asia. Mol Ecol 20:3414–3438PubMedCrossRefGoogle Scholar
  22. MacArthur RH (1967) The theory of island biogeography, vol 1. Princeton University Press, PrincetonGoogle Scholar
  23. MacArthur RH, Wilson EO (1963) An equilibrium theory of insular zoogeography. Evolution 17:373–387CrossRefGoogle Scholar
  24. Mayr E (1965) Avifauna: turnover on islands. Science 150:1587–1588PubMedCrossRefGoogle Scholar
  25. McKay BD (2012) A new timeframe for the diversification of Japan’s mammals. J Biogeogr 39:1134–1143CrossRefGoogle Scholar
  26. McKay BD, Mays HL, Peng YW, Kozak KH, Yao CT, Yuan HW (2010) Recent range-wide demographic expansion in a Taiwan endemic montane bird, Steere’s liocichla (Liocichla steerii). BMC Evol Biol 10:71PubMedPubMedCentralCrossRefGoogle Scholar
  27. Nishiumi I (2009) Population structure and origin of Japanese land birds. In: Higuchi H, Kuroda R (eds) Natural history of birds. Hokkaido University Press, Sapporo, pp 17–38 (in Japanese) Google Scholar
  28. Omland KE, Lanyon SM, Fritz SJ (1999) A molecular phylogeny of the New World orioles (Icterus): the importance of dense taxon sampling. Mol Phylogenet Evol 12:224–239PubMedCrossRefGoogle Scholar
  29. Päckert M, Martens J, Sun YH, Severinghaus LL, Nazarenko AA, Ting J, Töpfer T, Tietze DT (2012) Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes). J Biogeogr 39:556–573CrossRefGoogle Scholar
  30. Pavlova A, Zink RM, Drovetski SV, Red’kin Y, Rohwer S (2003) Phylogeographic patterns in Motacilla flava and Motacilla citreola: species limits and population history. Auk 120:744–758CrossRefGoogle Scholar
  31. Pavlova A, Zink RM, Rohwer S, Koblik EA, Red’kin YA, Fadeev IV, Nesterov EV (2005) Mitochondrial DNA and plumage evolution in the white wagtail Motacilla alba. J Avian Biol 36:322–336CrossRefGoogle Scholar
  32. Ratnasingham S, Hebert PD (2007) BOLD: the Barcode of Life Data System ( Mol Ecol Notes 7:355–364PubMedPubMedCentralCrossRefGoogle Scholar
  33. Saito Y, Yokoyama K, Tsutsumi Y, Tanimura Y (2006) Formation of the Japanese Islands. In: National Science Museum (ed) Natural history of the Japanese Islands. Tokai University Press, Tokyo, pp 23–40 (in Japanese)Google Scholar
  34. Saitoh T, Sugita N, Someya S, Iwami Y, Kobayashi S, Kamigaichi H, Higuchi A, Asai S, Yamamoto Y, Nishiumi I (2015) DNA barcoding reveals 24 distinct lineages as cryptic bird species candidates in and around the Japanese archipelago. Mol Ecol Res 15:177–186CrossRefGoogle Scholar
  35. Uramoto M (1973) Japan from the view of world bird distribution. Larousse Asahi Shimbun 134:47–50 (in Japanese) Google Scholar
  36. Wong EHK, Hanner RH (2008) DNA barcoding detects market substitution in North American seafood. Food Res Int 41:828–837CrossRefGoogle Scholar
  37. Yoo HS, Eah JY, Kim JS, Kim YJ, Min MS, Paek WK, Lee H, Kim CB (2006) DNA barcoding Korean birds. Mol Cells 22:323–327PubMedGoogle Scholar
  38. Zink RM, Drovetski SV, Rohwer S (2002) Phylogeographic patterns in the great spotted woodpecker Dendrocopos major across Eurasia. J Avian Biol 33:175–178CrossRefGoogle Scholar
  39. Zink RM, Drovetski SV, Rohwer S (2006) Selective neutrality of mitochondrial ND2 sequences, phylogeography and species limits in Sitta europaea. Mol Phylogenet Evol 40:679–686PubMedCrossRefGoogle Scholar
  40. Zink RM, Pavlova A, Drovetski S, Rohwer S (2008) Mitochondrial phylogeographies of five widespread Eurasian bird species. J Ornithol 149:399–413CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  1. 1.Department of ZoologyNational Museum of Nature and ScienceTsukubaJapan
  2. 2.Department of Nature SurveyNational Institute of EcologySeocheonRepublic of Korea

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