Environmental Biology of Fishes

, Volume 69, Issue 1–4, pp 37–50 | Cite as

Genetic Population Structure of Chum Salmon in the Pacific Rim Inferred from Mitochondrial DNA Sequence Variation

  • Shunpei Sato
  • Hiroyuki Kojima
  • Junko Ando
  • Hironori Ando
  • Richard L. Wilmot
  • Lisa W. Seeb
  • Vladimir Efremov
  • Larry LeClair
  • Wally Buchholz
  • Deuk-Hee Jin
  • Shigehiko Urawa
  • Masahide Kaeriyama
  • Akihisa Urano
  • Syuiti Abe
Article

Abstract

We examined the genetic population structure of chum salmon, Oncorhynchus keta, in the Pacific Rim using mitochondrial (mt) DNA analysis. Nucleotide sequence analysis of about 500 bp in the variable portion of the 5′ end of the mtDNA control region revealed 20 variable nucleotide sites, which defined 30 haplotypes of three genealogical clades (A, B, and C), in more than 2,100 individuals of 48 populations from Japan (16), Korea (1), Russia (10), and North America (21 from Alaska, British Columbia, and Washington). The observed haplotypes were mostly associated with geographic regions, in that clade A and C haplotypes characterized Asian populations and clade B haplotypes distinguished North American populations. The haplotype diversity was highest in the Japanese populations, suggesting a greater genetic variation in the populations of Japan than those of Russia and North America. The analysis of molecular variance and contingency χ2 tests demonstrated strong structuring among the three geographic groups of populations and weak to moderate structuring within Japanese and North American populations. These results suggest that the observed geographic pattern might be influenced primarily by historic expansions or colonizations and secondarily by low or restricted gene flow between local groups within regions. In addition to the analysis of population structure, mtDNA data may be useful for constructing a baseline for stock identification of mixed populations of high seas chum salmon.

mtDNA control region Pacific salmon haplotype genealogy genetic divergence 

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References

  1. Bandelt, H.J., P. Forster & A. Rohl. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37–48.Google Scholar
  2. Bernatchez, L., R. Guyomard & F. Bonhomme. 1992. DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Mol. Ecol. 1: 161–173.Google Scholar
  3. Bickham, J.W., C.C. Wood & J.C. Patton. 1995. Biogeographic implications of cytochrome b sequences and allozymes in sockeye (Oncorhynchus nerka). J. Hered. 86: 140–144.Google Scholar
  4. Brown, W.M., M. George, Jr. & A.C. Wilson. 1979. Rapid evolution of animal mitochondrial DNA. Proc. Natl Acad. Sci. U.S.A. 76: 1967–1971.Google Scholar
  5. Castelloe, J., & A.R. Templeton. 1994. Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol. Phylogen. Evol. 3: 102–113.Google Scholar
  6. Churikov, D., M. Matsuoka, X. Luan, A.K. Gray, V.A. Brykov & A.J. Gharrett. 2001. Assessment of concordance among genealogical reconstructions from various mtDNA segments in three species of Pacific salmon (genus Oncorhynchus). Mol. Ecol. 10: 2329–2339.CrossRefGoogle Scholar
  7. Cronin, M.A., W.J. Spearman, R.L. Wilmot, J.C. Patton & J.W. Bickham. 1993. Mitochondrial DNA variation in chinook (Oncorhynchus tshawytscha) and chum salmon (O. keta) detected by restriction enzyme analysis of polymerase chain reaction (PCR) products. Can. J. Fish. Aquat. Sci. 50: 708–715.Google Scholar
  8. Excoffier, L., P.E. Smouse & J.M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491.Google Scholar
  9. Ferguson, A., J.B. Taggart, P.A. Prodohl, O. Mcmeel, C. Thompson, C. Stone, P. Mcginnity & R.A. Hynes. 1995. The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo. J. Fish. Biol. 47(Suppl. A): 103–126.Google Scholar
  10. Gharrett, A.J., S.M. Shirley & G.R. Tromble. 1987. Genetic relationships among populations of Alaskan chinook salmon (Oncorhynchus tshawyscha). Can. J. Fish. Aquat. Sci. 44: 765–774.Google Scholar
  11. Hoelzel, A.R., J.M. Hancock & G.A. Dover. 1991. Evolution of the cetacean mitochondrial D-loop region. Mol. Biol. Evol. 8: 475–493.Google Scholar
  12. Kijima, A. & Y. Fujio. 1982. Correlation between geographic distance and genetic distance in populations of chum salmon Oncorhynchus keta. Bull. Jpn. Soc. Sci. Fish. 48: 1703–1709Google Scholar
  13. Kondzela, C.M., C.M. Guthrie, S.L. Hawkins, C.D. Russell, J.H. Helle & A.J. Gharrett. 1994. Genetic relationship among chum salmon populations in southeast Alaska and northern British Columbia. Can. J. Fish. Aquat. Sci. 51: 50–64.Google Scholar
  14. McElroy, D., P. Moran, E. Bermingham & I. Kornfield. 1993. REAP: An integrated environment for the manipulation and phylogenetic analysis of restriction data. J. Hered. 83: 157–158.Google Scholar
  15. Meyer, A. 1993. Evolution of mitochondrial DNA in fish. pp. 1–38. In: P.W. Hochachka & T.P. Mommsen (ed.) Biochemistry and Molecular Biology of Fishes, Vol. 2, Elsevier, Amsterdam.Google Scholar
  16. Moritz, C., T.E. Dowling & W.M. Brown. 1987. Evolution of animal mitochondrial DNA: Relevance for population biology and systematics. Ann. Rec. Ecol. Syst. 18: 269–292.Google Scholar
  17. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl Acad. Sci. U.S.A. 70: 3321–3323.Google Scholar
  18. Nei, M. & F. Tajima. 1981.DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.Google Scholar
  19. Nielsen, J.L., C. Gan & W.K. Thomas. 1994. Differences in genetic diversity for mitochondrial DNA between hatchery and wild population of Oncorhynchus. Can. J. Fish. Aquat. Sci. 51: 290–297.Google Scholar
  20. Okazaki, T. 1983. Genetic structure of chum salmon Oncorhynchus keta river populations. Bull. Jpn. Soc. Sci. Fish. 49: 189–196.Google Scholar
  21. Park, L.K., M.A. Brainard, D.A. Dightman & G.A.Winans. 1993. Low levels of intraspecific variation in the mitochondrial DNA of chum salmon (Oncorhynchus keta). Mol. Mar. Biol. Biotech. 2: 362–370.Google Scholar
  22. Phelps, S.R., L.L. Leclair, S. Young & H.L. Iankenship. 1994. Genetic diversity patterns of chum salmon in the Pacific northwest. Can. J. Fish. Aquat. Sci. 51(Suppl. 1): 65–83.Google Scholar
  23. Pigeon, D., J.J. Dodson & L. Bernatchez. 1998. A mtDNA analysis of spatiotemporal distribution of two sympatric larval populations of rainbow smelt (Osmerus mordax) in the St. Lawrence River estuary, Quebec, Canada. Can. J. Fish. Aquat. Sci. 55: 1739–1747.CrossRefGoogle Scholar
  24. Posada, D. & K.A. Crandall. 2001.Intraspecific gene genealogies: Trees grafting into networks. Trends. Ecol. Evol. 16: 37–45.CrossRefGoogle Scholar
  25. Roff, D.A. & P. Bentzen. 1989. The statistical analysis of mitochondrial DNA polymorphisms: Chi 2 and the problem of small samples. Mol. Biol. Evol. 6: 539–545.Google Scholar
  26. Saitou, N. & M. Nei. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.Google Scholar
  27. Salo, E.O. 1991. Life history of chum salmon (Oncorhynchusketa). pp. 231–309. In: C. Groot & L. Margolis (ed.) Pacific Salmon Life Histories. University of British Columbia Press, Vancouver.Google Scholar
  28. Sambrook, J., E.F. Fritsch & T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd edition, Cold Spring Harbor Laboratory Press, New York. 9.16–9.23.Google Scholar
  29. Sato, S., J. Ando, H. Ando, S. Urawa, A. Urano & S. Abe. 2001. Genetic variation among Japanese populations of chum salmon inferred from the nucleotide sequences of the mitochondrial DNA control region. Zool. Sci. 18: 99–106.Google Scholar
  30. Seeb, L.W. & P.A. Crane. 1999a. High genetic heterogeneity in chum salmon in western Alaska, the contact zone between northern and southern lineages. Trans. Am. Fish. Soc. 128: 58–87.Google Scholar
  31. Seeb, L.W. & P.A. Crane. 1999b. Allozymes and mitochondrial DNA discriminate Asian and north American populations of chum salmon in mixed-stock fisheries along the south coast of the Alaska Peninsula. Trans. Am. Fish. Soc. 128: 88–103.Google Scholar
  32. Taylor, E.B., T.D. Beacham & M. Kaeriyama. 1994. Population structure and identification of north Pacific Ocean chum salmon (Oncorhynchus keta) revealed by an analysis of minisatellite DNA variation. Can. J. Fish. Aquat. Sci. 51: 1430–1442.Google Scholar
  33. Templeton, A.R., K.A. Crandall & C.F. Sing. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619–633.Google Scholar
  34. Utter, F.M., Campton, D., Grant, S., Milner, G., Seeb, J. & L. Wishard. 1980. Population structure of indigenous salmonid species of the Pacific northwest. pp. 285–304. In: W.J. McNeil & D.C. Himsworth (ed.) Salmonid ecosystems of the North Pacific. Oregon State University Press, Corvallis.Google Scholar
  35. Varnavskaya, N.V. & T.D. Beacham. 1992. Biochemical genetic variation in odd-year pink salmon (Oncorhynchus gorbuscha) from Kamchatka. Can. J. Zool. 70: 2115–2120.Google Scholar
  36. Varnavskaya, N.V., C.C. Wood, R.J. Everett, R.L.Wilmot, V.S.Varnavsky, V.V. Midanaya & T.P. Quinn. 1994. Genetic differentiation of subpopulations of sockeye salmon (Oncorhynchus nerka) within lakes of Alaska, British Columbia, and Kamchatka, Russia. Can. J. Fish. Aquat. Sci. 51(Suppl. 1): 147–157.Google Scholar
  37. Wilmot, R.L., R.J. Everett, W.J. Spearman, R. Baccus, N.V. Varnavskaya & S.V. Putivkin. 1994. Genetic stock structure of western Alaska chum salmon and a comparison with Russia far east stocks. Can. J. Fish. Aquat. Sci. 51(Suppl. 1): 84–94.Google Scholar
  38. Wilmot, R.L., C.M. Kondzela, C.M. Guthrie & M.M. Masuda. 1998. Genetic stock identification of chum salmon harvested incidentally in the 1994 and 1995 Bering Sea trawl fishery. N. Pac. Anadr. Fish. Comm. Bull. 1: 285–299.Google Scholar
  39. Wilson, G.M., W.K. Thomas & A.T. Beckenbach. 1987. Mitochondrial DNA analysis of Pacific northwest populations of Oncorhynchus tshawytscha. Can. J. Fish. Aquat. Sci. 44: 1301–1305.Google Scholar
  40. Winans, G.A., P.B. Aebersold, S. Urawa & N.V. Varnavskaya. 1994. Determining continent of origin of chum salmon (Oncorhynchus keta) using genetic stock identification techniques: Status of allozyme baseline in Asia. Can. J. Fish. Aquat. Sci. 51: 95–113.Google Scholar
  41. Zaykin, D.V. & A.I. Pudovkin. 1993. Two programs to estimate significance of ? 2 values using pseudo-probability tests. J. Hered. 84: 152.Google Scholar
  42. Zhivotovsky, L.A., A.J. Gharrett, A.J. MacGregor, M.K. Glubokovsky & M.W. Feldman. 1994. Gene differentiation in Pacific salmon (Oncorhynchus sp.): Facts and models with reference to pink salmon (O. gorbuscha). Can. J. Fish. Aquat. Sci. 51: 223–232.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Shunpei Sato
    • 1
  • Hiroyuki Kojima
    • 2
  • Junko Ando
    • 1
  • Hironori Ando
    • 1
  • Richard L. Wilmot
    • 3
  • Lisa W. Seeb
    • 4
  • Vladimir Efremov
    • 5
  • Larry LeClair
    • 6
  • Wally Buchholz
    • 7
  • Deuk-Hee Jin
    • 8
  • Shigehiko Urawa
    • 9
  • Masahide Kaeriyama
    • 2
  • Akihisa Urano
    • 1
    • 10
  • Syuiti Abe
    • 11
    • 12
  1. 1.Division of Biological Science, Graduate School of ScienceHokkaido UniversitySapporoJapan
  2. 2.Graduate School of Science and EngineeringHokkaido Tokai UniversitySapporoJapan
  3. 3.Auke Bay LaboratoryAlaska Fisheries Science Center, NOAAJuneauU.S.A.
  4. 4.Alaska Department of Fish and GameAnchorageU.S.A.
  5. 5.Russian Academy of ScienceVladivostokRussia
  6. 6.Washington Department of Fish and WildlifeOlympiaU.S.A.
  7. 7.U.S. Fish and Wildlife ServiceAnchorageU.S.A.
  8. 8.Kangnung National UniversityKangnungKorea
  9. 9.Salmon Resources CenterSapporoJapan
  10. 10.Field Science CenterHokkaido UniversitySapporoJapan
  11. 11.Laboratory of Animal Cytogenetics, Center for Advanced Science and TechnologyHokkaido UniversitySapporoJapan
  12. 12.Laboratory of Breeding Science, Graduate School of Fisheries SciencesHokkaido UniversityHakodateJapan

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