Conservation Genetics

, Volume 13, Issue 1, pp 143–151 | Cite as

Inferring the ancient population structure of the vulnerable albatross Phoebastria albatrus, combining ancient DNA, stable isotope, and morphometric analyses of archaeological samples

  • Masaki Eda
  • Hiroko Koike
  • Masaki Kuro-o
  • Shozo Mihara
  • Hiroshi Hasegawa
  • Hiroyoshi Higuchi
Research Article


The history of population structure is a key to effective wildlife management and conservation. However, inferring the history of population structure using present genetic structures is problematic when the method is applied to species that have experienced severe population bottlenecks. Ancient DNA analysis seemed to be a promising, direct method for inferring ancient population structures. However, the usual methods for inferring modern population structure, i.e. the phylogeographic approach using mitochondrial DNA and the Bayesian approach using microsatellite DNA, are often unsuitable for ancient samples. In this study, we combined ancient DNA obtained from zooarchaeological bones with carbon/nitrogen stable isotope ratios and morphological variations to infer ancient population structure of the short-tailed albatross Phoebastria albatrus. The results showed that the bird existed in two populations, between which the genetic distance was greater than that of distinct sister albatross species, although no subspecies of P. albatrus have been proposed. Our results suggest that the birds at the present two breeding regions (Torishima in the Izu Islands and two islets of the Senkaku Islands) are descended from these two ancient populations, and that reevaluation of the status and conservation strategy for the species is required. Our results also indicate that lineage breeding on the Senkaku Islands has drastically reduced genetic diversity, while that on Torishima has not. The approach proposed in this study would be useful for inferring ancient population structure, using samples of highly mobile animals and/or samples from archaeological sites, and the reconstructed ancient population structure would be useful for conservation and management recommendations.


Ancient DNA Archaeological materials Phoebastria albatrus Population structure Stable isotope analysis Short-tailed albatross 



We thank Dr. Ushio Maeda for use of the albatross bones from HM2. We also thank Drs. Go Fujita, Tadashi Miyashita, Gregory Balogh, Haruki Tatsuta, Yoko Kunitake, Masaki Fujita, and Tatsuya Amano for their insightful comments on the manuscript and Dr. Van’t Hof and Jiro Eda for improving our English. Helpful comments from two anonymous reviewers clarified the strengths and weaknesses of this study. This study was supported financially in part by a Grant-in-Aid for JSPS Fellows to ME from the Japan Society for the Promotion of Science (No. 16-6316).

Supplementary material

10592_2011_270_MOESM1_ESM.pdf (86 kb)
Supplementary material 1 (PDF 86 kb)


  1. Abbott CL, Double MC (2003) Phylogeography of shy and white-capped albatrosses inferred from mitochondrial DNA sequences: implications for population history and taxonomy. Mol Ecol 12:2747–2758. doi: 10.1046/j.1365-294X.2003.01944.x PubMedCrossRefGoogle Scholar
  2. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  3. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography—the mitochondrial-DNA bridge between population-genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  4. BirdLife International (2008) Phoebastria albatrus. Accessed 22nd July 2009
  5. Burg TM, Croxall JP (2001) Global relationships amongst black-browed and grey-headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites. Mol Ecol 10:2647–2660PubMedCrossRefGoogle Scholar
  6. Burg TM, Croxall JP (2004) Global population structure and taxonomy of the wandering albatross species complex. Mol Ecol 13:2345–2355. doi: 10.1111/j.1365-294X.2004.02232.x PubMedCrossRefGoogle Scholar
  7. Chamberlain CP, Blum JD, Holmes RT, Feng XH, Sherry TW, Graves GR (1997) The use of isotope tracers for identifying populations of migratory birds. Oecologia 109:132–141CrossRefGoogle Scholar
  8. Clegg SM, Kelly JF, Kimura M, Smith TB (2003) Combining genetic markers and stable isotopes to reveal population connectivity and migration patterns in a Neotropical migrant, Wilson’s warbler (Wilsonia pusilla). Mol Ecol 12:819–830PubMedCrossRefGoogle Scholar
  9. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  10. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  11. DeNiro MJ (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Science 317:806–809Google Scholar
  12. Deniro MJ, Epstein S (1978) Influence of diet on distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  13. Deniro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  14. Development Core Team R (2009) R: a language and environment for statistical computing., 2.10.1 edn. R Foundation for Statistical Computing, ViennaGoogle Scholar
  15. Driesch A (1976) A guide to the measurements of animal bones from archaeological sites. Peabody Museum Bull 1:1–136Google Scholar
  16. Eda M, Koike H, Sato F, Higuchi H (2005) Why were so many albatross remains found in northern Japan? In: Grupe G, Peters J (eds) Feathers, grit and symbolism: birds and humans in the old and new worlds. Verlag Marie Leidorf GmbH, Westfalen, pp 131–140Google Scholar
  17. Eda M, Baba Y, Koike H, Higuchi H (2006) Do temporal size differences influence species identification of archaeological albatross remains when using modern reference samples? J Archaeol Sci 33:349–359. doi: 10.1016/j.jas.2005.07.017 CrossRefGoogle Scholar
  18. Eda M, Kuro-o M, Higuchi H, Hasegawa H, Koike H (2010) Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidae (albatrosses). Genes Genet Syst 85:129–139PubMedCrossRefGoogle Scholar
  19. Excoffier L, Schneider S (1999) Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602PubMedCrossRefGoogle Scholar
  20. Fox CW, Roff DA, Fairbairn DJ (2001) Evolutionary ecology. Oxford University Press, OxfordGoogle Scholar
  21. Futuyma DJ (1986) Evolutionary Biology. Sinauer Association Inc., SunderlandGoogle Scholar
  22. Hadly EA, Kohn MH, Leonard JA, Wayne RK (1998) A genetic record of population isolation in pocket gophers during Holocene climatic change. Proc Natl Acad Sci USA 95:6893–6896PubMedCrossRefGoogle Scholar
  23. Hardy C, Callou C, Vigne JD, Casane D, Dennebouy N, Mounolou JC, Monnerot M (1995) Rabbit mitochondrial DNA diversity from prehistoric to modern times. J Mol Evol 40:227–237PubMedCrossRefGoogle Scholar
  24. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Association Inc., SunderlandGoogle Scholar
  25. Hasegawa H (2003) From fifty to five thousands: for the restoration of the short-tailed albatross. Doubutsu-sha, Tokyo (in Japanese)Google Scholar
  26. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  27. Hobson KA, Wassenaar LI (1997) Linking breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopic analysis of feathers. Oecologia 109:142–148CrossRefGoogle Scholar
  28. Hofreiter M, Jaenicke V, Serre D, von Haeseler A, Paabo S (2001) DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res 29:4793–4799PubMedCrossRefGoogle Scholar
  29. Inchausti P, Weimerskirch H (2002) Dispersal and metapopulation dynamics of an oceanic seabird, the wandering albatross, and its consequences for its response to long-line fisheries. J Animal Ecol 71:765–770CrossRefGoogle Scholar
  30. Jaenicke-Despres V, Buckler ES, Smith BD, Gilbert MTP, Cooper A, Doebley J, Paabo S (2003) Early allelic selection in maize as revealed by ancient DNA. Science 302:1206–1208PubMedCrossRefGoogle Scholar
  31. Klicka J, Zink RM, Barlow JC, McGillivray WB, Doyle TJ (1999) Evidence supporting the recent origin and species status of the Timberline Sparrow. Condor 101:577–588CrossRefGoogle Scholar
  32. Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol Ecol 11:2623–2635PubMedCrossRefGoogle Scholar
  33. Kuro-o M, Yonekawa H, Saito S, Eda M, Higuchi H, Koike H, Hasegawa H (2010) Unexpectedly high genetic diversity of mtDNA control region through severe bottleneck in vulnerable albatross Phoebastria albatrus. Conserv Genet 11:127–137CrossRefGoogle Scholar
  34. Lawrence HA, Scofield RP, Crockett DE, Millar CD, Lambert DM (2008) Ancient genetic variation in one of the world’s rarest seabirds. Heredity 101:543–547. doi: 10.1038/hdy.2008.85 PubMedCrossRefGoogle Scholar
  35. Leonard JA (2008) Ancient DNA applications for wildlife conservation. Mol Ecol 17:4186–4196. doi: 10.1111/j.1365-294X.2008.03891.x PubMedCrossRefGoogle Scholar
  36. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi: 10.1093/bioinformatics/btp187 PubMedCrossRefGoogle Scholar
  37. Lott CA, Meehan TD, Heath JA (2003) Estimating the latitudinal origins of migratory birds using hydrogen and sulfur stable isotopes in feathers: influence of marine prey base. Oecologia 134:505–510. doi: 10.1007/s00442-002-1153-8 PubMedGoogle Scholar
  38. Maeda U, Yamaura K (1992) Excavation research of Hamanaka 2 site. Maeda Insatsu, Tsukuba (in Japanese)Google Scholar
  39. Mihara S, Okuno M, Ogawa H, Tanaka K, Nakamura T, Koike H (2002) AMS 14-C dating and dietary analysis for Lal-lo shell midden sites, Philippines. Summ Res Using AMS Nagoya Univ 13:82–104 (in Japanese)Google Scholar
  40. Moore PJ, Taylor GA, Amey JM (1997) Interbreeding of black-browed albatross Diomedea m. melanophris and New Zealand black-browed albatross D. m. impavida on Campbell Island. Emu 97:322–324CrossRefGoogle Scholar
  41. Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  42. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  43. Prum B, Guilloudbataille M, Clergetdarpoux F (1990) On the use of chi-2 tests for nested categorized data. Ann Hum Genet 54:315–320PubMedCrossRefGoogle Scholar
  44. Rains D, Weimerskirch H, Burg TM (2011) Piecing together the global population puzzle of wandering albatrosses: genetic analysis of the Amsterdam albatross Diomedea amsterdamensis. J Avian Biol 42:69–79. doi: 10.1111/j.1600-048X.2010.05295.x CrossRefGoogle Scholar
  45. Ramakrishnan U, Hadly EA (2009) Using phylochronology to reveal cryptic population histories: review and synthesis of 29 ancient DNA studies. Mol Ecol 18:1310–1330. doi: 10.1111/j.1365-294X.2009.04092.x PubMedCrossRefGoogle Scholar
  46. Rasmussen PC (1994) Geographic-variation in morphology and allozymes of south-american imperial shags. Auk 111(1):143–161Google Scholar
  47. Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW (2002) Genetic structure of human populations. Science 298:2381–2385PubMedCrossRefGoogle Scholar
  48. Shepherd LD, Millar CD, Ballard G, Ainley DG, Wilson PR, Haynes GD, Baroni C, Lambert DM (2005) Microevolution and mega-icebergs in the Antarctic. Proc Natl Acad Sci USA 102:16717–16722. doi: 10.1073/pnas.0502281102 PubMedCrossRefGoogle Scholar
  49. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599. doi: 10.1093/molbev/msm092 Google Scholar
  50. Templeton AR (1993) The “Eve” hypothesis: a genetic critique and reanalysis. Am Anthropol 95:51–72CrossRefGoogle Scholar
  51. Templeton A, Georgiadis RNJ (1995) A landscape approach to conservation genetics: conserving evolutionary processes in the African Bovidae. In: Avise JC, Hamrick JL (eds) Conservation genetics. Chapman & Hall, New York, pp 398–430Google Scholar
  52. Templeton AR, Sing CF (1993) A cladistic-analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669PubMedGoogle Scholar
  53. Templeton AR, Sing CF, Kessling A, Humphries S (1988) A cladistic analysis of phenotype associations with haplotypes inferred from restriction endonuclease mapping. II. The analysis of natural populations. Genetics 120:1145–1154PubMedGoogle Scholar
  54. Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767–782PubMedGoogle Scholar
  55. Tickell WLN (2000) Albatrosses. Yale University Press, New HaevenGoogle Scholar
  56. U. S. Fish and Wildlife Service (2008) Short-tailed albatross recovery plan.1-105Google Scholar
  57. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Masaki Eda
    • 1
    • 5
  • Hiroko Koike
    • 2
    • 6
  • Masaki Kuro-o
    • 3
  • Shozo Mihara
    • 2
    • 7
  • Hiroshi Hasegawa
    • 4
  • Hiroyoshi Higuchi
    • 1
  1. 1.School of Agriculture and Life SciencesUniversity of TokyoTokyoJapan
  2. 2.Graduate School of Social and Cultural StudiesKyushu UniversityFukuokaJapan
  3. 3.Department of BiologyHirosaki UniversityAomoriJapan
  4. 4.Biology DepartmentToho UniversityChibaJapan
  5. 5.Faculty of MedicineTottori UniversityTottoriJapan
  6. 6.The Kyushu University MuseumFukuokaJapan
  7. 7.Faculty of Urban Liberal ArtsTokyo Metropolitan UniversityTokyoJapan

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