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Intraspecific polymorphism of mtDNA in Sakhalin taimen Parahucho perryi

  • Animal Genetics
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Abstract

The intraspecific polymorphism of Sakhalin taimen Parahucho perryi (Brevoort, 1856), Salmonidae, was assessed via the RFLP analysis of mitochondrial DNA fragments that contain Cytb, the control region (D loop), and the genes for the NADH dehydrogenase subunits 1–4, as well as the sequencing of the mitochondrial DNA COI gene. The statistically significant differentiation of the populations from the mainland coast of the Sea of Japan and the eastern and western coasts of Sakhalin Island was demonstrated. The higher level of haplotype diversity in Sakhalin populations compared to Primorye populations and the structure of haplotype genealogies suggested that all populations of Parahucho perryi originated from a common ancestor, which probably lived on the western coast of the Sakhalin Island.

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References

  1. Berg, L.S., Ryby presnykh vod SSSR i sopredel’nykh stran (Freshwater Fishes of the Soviet Union and Adjacent Countries), Moscow: Izd. Akad. Nauk SSSR, 1948, part 1, 4th ed.

    Google Scholar 

  2. Zolotukhin, S.F., Semenchenko, A.Yu., and Belyaev, V.A., Taimeni i lenki Dal’nego Vostoka Rossii (Taimen and Lenok of Russian Far East), Khabarovsk: Khabarovskaya kraevaya tipografiya, 2000.

    Google Scholar 

  3. Zolotukhin, S.F., Kryukova, M.V., and Kulikov, A.N., Zhemchuzhiny nashei prirody: Reka Koppi (Pearls of Our Nature: The Koppi River), Khabarovsk: Tipografiya Zhaso Amur, 2010.

    Google Scholar 

  4. Semenchenko, A.Yu. and Zolotukhin, S.F., Reproduction effectiveness of Sakhalin taimen (Parahucho perryi) in the Sakhalin Rivers and the strategy of their Conservation, in Chteniya pamyati Vladimira Yakovlevicha Levanidova (Readings in Memoriam of Vladimir Yakovlevich Levanidov), Vladivostok: Dal’nauka, 2011, no. 5, pp. 472–482.

    Google Scholar 

  5. Zimmerman, C.E., Rand, P.S., Fukushima, M., and Zolotukhin, S.F., Migration of Sakhalin taimen (Parahucho perryi): evidence of freshwater resident life history types, Environ. Biol. Fish, DOI 10.1007/s10641011-9908-x

  6. Klyuchareva, O.A., Ichtyofauna of lagoon lakes of Kunashir island (the Kuril Islands), Zool. Zh., 1967, vol. 46, no. 3, pp. 384–392.

    Google Scholar 

  7. Gritsenko, O.F. and Churikov, A.A., Geographic and size variation of Sakhalin taimen Hucho perryi (Brevoort), in Lososevidnye ryby (Salmonid Fishes), Leningrad: Nauka, 1980, pp. 92–100.

    Google Scholar 

  8. Parpura, I.Z., Comparative morphobiological descriptions of Sakhalin taimen from the waters of northern Primorye, in Biologiya shel’fovykh i prokhodnykh ryb (Biology of Shelf and Anadromous Fish Species), Vladivostok: Dal’nevost. Otd. Ross. Akad. Nauk, 1990, pp. 39–46.

    Google Scholar 

  9. Semenchenko, A.Yu., The Samarga River fishes (Primorsky Krai), in Chteniya pamyati Vladimira Yakovlevicha Levanidova (Readings in Memoriam of Vladimir Yakovlevich Levanidov), Vladivostok: Dal’nauka, 2003, no. 2, pp. 337–354.

    Google Scholar 

  10. Edo, K., Kawaguchi, Y., Nunokawa, M., et al., Morphology, stomach contents and growth of the endangered salmonid, Sakhalin taimen Hucho perryi, captured in the sea of Okhotsk, northern Japan: evidence of an anadromous form, Environ. Biol. Fish, 2005, vol. 74, pp. 1–7.

    Article  Google Scholar 

  11. Gritsenko, O.F. and Klovach, N.V., Soobshchestvo ryb Nyiskogo zaliva (Severo-Vostochnyi Sakhalin) v 1972–1974 gg. do nachala neftegazovykh razrabotok (Fish Community of the Nyisky Bay (Northwestern Sakhalin) 1972–1974 prior to Oil and Gas Development), Moscow: VNIRO, 2006.

    Google Scholar 

  12. Zolotukhin, S.F. and Semenchenko, A.Yu., Growth and distribution of Sakhalin taimen Hucho perryi (Brevoort) in river basins, in Chteniya pamyati Vladimira Yakovlevicha Levanidova (Readings in Memoriam of Vladimir Yakovlevich Levanidov), Vladivostok: Dal’nauka, 2008, no. 4, pp. 317–338.

    Google Scholar 

  13. Esteve, M., McLennan, D.A., and Kawahara, M., Spawning behavior of Sakhalin taimen, Parahucho perryi, from northern Hokkaido, Japan, Environ. Biol. Fish, 2009, vol. 85, pp. 265–273.

    Article  Google Scholar 

  14. Honda, K., Arai, T., Takahashi, N., and Miyashita, K., Life history and migration of Sakhalin taimen Hucho perryi, caught from lake Akkeshi in eastern Hokkaido, Japan, as revealed by Sr: Ca ratios of otoliths, Ichthyol. Res., 2010, vol. 57, pp. 416–421.

    Article  Google Scholar 

  15. Nomoto, K., Omiya, H., Sugimoto, T., et al., Potential negative impacts of introduced rainbow trout on endangered Sakhalin taimen through redd disturbance in an agricultural stream, eastern Hokkaido, Ecol. Freshwater Fish, 2010, vol. 19, pp. 116–126.

    Article  Google Scholar 

  16. Fukushima, M., Shimazaki, H., Rand, P.S., and Kaeriyama, M., Reconstructing Sakhalin taimen Parahucho perryi historical distribution and identifying causes for local extinctions, Trans. Am. Fish. Soc., 2011, vol. 140, pp. 1–13.

    Google Scholar 

  17. Osinov, A.G., Genetic divergence and phylogenetic interrelationships between lenoks of the genus Brachymystax and taimens of the genera Hucho and Parahucho, Genetika (Moscow), 1991, vol. 27, no. 12, pp. 2127–2136.

    Google Scholar 

  18. Oleinik, A.G. and Polyakova, N.E., Analiz mezhvidovoi geneticheskoi differentsiatsii u nekotorykh vidov sem. Salmonidae (Analysis of Interspecies Genetic Differentiation among Some Species of the Family Salmonidae), Available from VINITI, 1992, Moscow, nos. 1317–1392.

    Google Scholar 

  19. Hatakeyama, M., Watanabe, T., Ikeda, M., et al., Isolation and characterization of microsatellite DNA loci for endangered fish, Japanese huchen (Hucho perryi), Mol. Ecol. Notes, 2005, vol. 5, pp. 893–895.

    Article  CAS  Google Scholar 

  20. Oleinik, A.G. and Skurikhina, L.A., Phylogenetic relationships of Sakhalin taimen, Parahucho perryi inferred from PCR-RFLP analysis of mitochondrial DNA, Russ. J. Genet., 2008, vol. 44, no. 7, pp. 767–776.

    Article  CAS  Google Scholar 

  21. Kopun, Th., Winkler, K.A., and Weiss, S., Eight new polymorphic microsatellite DNA markers for Sakhalin taimen, Parahucho perryi, Conserv. Genet., 2009, vol. 10, pp. 1089–1091.

    Article  CAS  Google Scholar 

  22. Shitova, M.V., Yurchenko, A.A., Shaykhaeva, E.G., and Zhivotovsky, L.A., A panel of microsatellite loci for population studies of Sakhalin taimen, Parahucho perryi (Brevoort), Russ. J. Genet., 2012, vol. 48, no. 8, pp. 831–837.

    Article  CAS  Google Scholar 

  23. Krasnaya kniga Sakhalinskoi oblasti: Ryby (Red Book of Sakhalin Oblast: Fishes), Yuzhno-Sakhalinsk: Sakhalinskoe knizhnoe izd., 2000.

  24. Krasnaya kniga Rossiiskoi Federatsii (zhivotnye) (Red Book of the Russian Federation (Animals)), Moscow: Astrel’, 2001.

  25. IUCN Red List of Threatened Species, 2007. http://www.iucnredlist.org

  26. Zardoya, R. and Meyer, A., Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates, Mol. Biol. Evol., 1996, vol. 13, no. 7, pp. 933–942.

    Article  PubMed  CAS  Google Scholar 

  27. Hebert, P.D.N., Cywinska, A., and Ball, S.L., Biological identifications through DNA barcodes, Proc. R. Soc. London, Ser. B, 2003, vol. 270, pp. 313–321.

    Article  CAS  Google Scholar 

  28. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1989, 2nd ed.

    Google Scholar 

  29. Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Divergence of the Salvelinus species mitochondrial DNA from Northeastern Asia, Ecol. Freshwater Fish, 2007, vol. 16, no. 1, pp. 87–98.

    Article  Google Scholar 

  30. Ward, R.D., Zemlak, T.S., Innes, B.H., et al., DNA barcoding Australia’s fish species, Philos. Trans. R. Soc., B, 2005, vol. 360, no. 1462, pp. 1847–1857.

    Article  CAS  Google Scholar 

  31. Skurikhina, L.A., Kukhlevsky, A.D., Oleinik, A.G., and Kovpak, N.E., Phylogenetic analysis of smelts (Osmeridae) based on the variation of cytochrome b gene, Russ. J. Genet., 2010, vol. 46, no. 1, pp. 69–80.

    Article  CAS  Google Scholar 

  32. Kovpak, N.E., Skurikhina, L.A., Kukhlevsky, A.D., et al., Genetic divergence and relationships among smelts of the genus Osmerus from the Russian waters, Russ. J. Genet., 2011, vol. 47, no. 8, pp. 958–972.

    Article  CAS  Google Scholar 

  33. McElroy, D., Moran, P., Bermingham, E., and Kornfield, I., REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data, J. Hered., 1992, vol. 83, pp. 153–158.

    Google Scholar 

  34. Excoffier, L. and Lischer, H.E.L., Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, pp. 564–567.

    Article  PubMed  Google Scholar 

  35. Nei, M. and Tajima, F., DNA polymorphism detectable by restriction endonucleases, Genetics, 1981, vol. 97, pp. 145–163.

    PubMed  CAS  Google Scholar 

  36. Nei, M. and Miller, J.C., A simple method for estimating average number of nucleotide substitution within and between populations from restriction data, Genetics, 1990, vol. 125, pp. 837–879.

    Google Scholar 

  37. Roff, D. and Bentzen, P., The statistical analysis of mitochondrial DNA polymorphisms: chi-square and the problem of small samples, Mol. Biol. Evol., 1989, vol. 5, pp. 539–545.

    Google Scholar 

  38. Excoffier, L., Smouse, P.E., and Quattro, J.M., Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data, Genetics, 1992, vol. 131, pp. 479–491.

    PubMed  CAS  Google Scholar 

  39. Rodgers, A.R. and Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, vol. 9, pp. 552–569.

    Google Scholar 

  40. Harpending, H.C., Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution, Hum. Biol., 1994, vol. 66, no. 4, pp. 591–600.

    PubMed  CAS  Google Scholar 

  41. Weir, B.S. and Cockerham, C.C., Estimating F-statistics for the analysis of population structure, Evolution, 1984, vol. 38, pp. 1358–1370.

    Article  Google Scholar 

  42. Weir, B.S., Genetic Data Analysis II: Methods for Discrete Population Genetic Data, Sunderland: Sinauer Associates, 1996, 2nd ed.

    Google Scholar 

  43. Swofford, D.L., PAUP*. Phylogenetic Analysis Using Parsinomy (*and Other Methods): Beta Version 10, Sunderland: Sinauer Associates, 2002.

    Google Scholar 

  44. Felsenstein, J., PHYLIP (Phylogeny Inference Package) version 3.67, University of Washington, 2007.

    Google Scholar 

  45. Felsenstein, J., Confidence limits on phylogenies: an approach using bootstrap, Evolution, 1985, vol. 39, pp. 783–791.

    Article  Google Scholar 

  46. Bandelt, H.-J., Foster, P., and Rohl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 1999, vol. 16, pp. 37–48.

    Article  PubMed  CAS  Google Scholar 

  47. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, pp. 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  48. Posada, D., jModelTest: phylogenetic model averaging, Mol. Biol. Evol., 2008, vol. 25, pp. 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  49. Tamura, K. and Nei, M., Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees, Mol. Biol. Evol., 1993, vol. 10, no. 3, pp. 512–526.

    PubMed  CAS  Google Scholar 

  50. Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, no. 4, pp. 406–425.

    PubMed  CAS  Google Scholar 

  51. Tamura, K., Peterson, D., Peterson, N., et al., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 28, pp. 2731–2739.

    Article  PubMed  CAS  Google Scholar 

  52. Sober, E., Parsimony in systematics: philosophical issues, Ann. Rev. Ecol. Syst., 1983, vol. 14, pp. 335–357.

    Article  Google Scholar 

  53. Huson, D.H. and Bryant, D., Application of phylogenetic networks in evolutionary studies, Mol. Biol. Evol., 2006, vol. 23, no. 2, pp. 254–267. www.splitstree.org/

    Article  PubMed  CAS  Google Scholar 

  54. Avise, J.C., Phylogeography: The History and Formation of Species, Cambridge: Harvard Univ. Press, 2000.

    Google Scholar 

  55. Nei, M., Maruyama, T., and Chakraborty, R., The bottleneck effect and genetic variation in populations, Evolution, 1975, vol. 29, pp. 1–10.

    Article  Google Scholar 

  56. Ibrahim, K.M., Nichols, R.A., and Hewitt, G.M., Spatial patterns of genetic variation generated by different forms of dispersal during range expansion, Heredity, 1996, vol. 77, pp. 282–291.

    Article  Google Scholar 

  57. Costello, A.B., Down, T.E., Pollard, S.M., et al., The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae), Evolution, 2003, vol. 57, pp. 328–344.

    PubMed  CAS  Google Scholar 

  58. Taylor, E.B., Stamford, M.D., and Baxter, J.S., Population subdivision in west slope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications, Mol. Ecol., 2003, vol. 12, pp. 2609–2622.

    Article  PubMed  CAS  Google Scholar 

  59. Stamford, M.D. and Taylor, E.B., Phylogeographical lineages of Arctic grayling (Thymallus arcticus) in North America: divergence, origins, and affinities with Eurasian Thymallus, Mol. Ecol., 2004, vol. 13, pp. 1533–1549.

    Article  PubMed  CAS  Google Scholar 

  60. Bushuev, V.P., Biology of taimen, Hucho perryi (Brevoort) from the Kievka River (southern Primorye), in Ekologiya i sistematika presnovodnykh organizmov Dal’nego Vostoka (Ecology and Systematics of Freshwater Organisms of the Russian Far East), Vladivostok: Dal’nevost. Nauch. Tsentr Ross. Akad. Nauk SSSR, 1983, pp. 61–72.

    Google Scholar 

  61. Glubokovskii, M.K., Evolyutsionnaya biologiya lososevykh ryb (Evolutionary Biology of Salmonid Fishes), Moscow: Nauka, 1995.

    Google Scholar 

  62. Crespi, B.J. and Fulton, M.J., Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny, Mol. Phylogenet. Evol., 2004, vol. 31, pp. 658–679.

    Article  PubMed  CAS  Google Scholar 

  63. Matveev, V., Nishihara, H., and Okada, N., Novel SINE families from salmons validate Parahucho (Salmonidae) as a distinct genus and give evidence that SINEs can incorporate line-related 3′-tails of other SINEs, Mol. Biol. Evol., 2007, vol. 24, pp. 1656–1666.

    Article  PubMed  CAS  Google Scholar 

  64. Shedko, S.V., Miroshnichenko, I.L., and Nemkova, G.A., Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of nuclear RAG 1 gene, Russ. J. Genet., 2012, vol. 48, no. 5, pp. 575–579.

    Article  CAS  Google Scholar 

  65. Nazarkin, M.V., Miocene fishes from of Agnevsk suite of Sakhalin Island: fauna, systematics, and origin, Extended Abstract of Cand. Sci. (Biol.) Dissertation, St. Petersburg: St. Petersburg Gos. Univ., 2000.

    Google Scholar 

  66. Lindberg, G.U., Krupnye kolebaniya urovnya okeana v chetvertichnyi period (Large Fluctuations of the Ocean Level in the Quaternary), Leningrad: Nauka, 1972.

    Google Scholar 

  67. Kulakov, A.P., Chetvertichnye beregovye linii Okhotskogo i Yaponskogo morei (Quaternary Shorelines of the Seas of Okhotsk and Japan), Novosibirsk: Nauka, 1973.

    Google Scholar 

  68. Aleksandrova, A.N., Pleistotsen Sakhalina (Pleistocene of Sakhalin), Moscow: Nauka, 1982.

    Google Scholar 

  69. Gladenkov, Yu.B., Bazhenova, O.K., Grechin, V.I., et al., Kainozoi Sakhalina i ego neftegazonosnost (Cenozoic of Sakhalin and Its Oil-and-Gas Content), Moscow: GEOS, 2002.

    Google Scholar 

  70. Korotkii, F.M., Pushkar’, V.S., and Grebennikova, T.A., Morskie terrasy i chetvertichnaya istoriya shel’fa Sakhalina (Sea Terraces and Quaternary History of the Sakhalin Shelf), Vladivostok: Dal’nauka, 1997.

    Google Scholar 

  71. Brovko, P.F., Lagoons as indicators of paleogeographic barriers, in Paleogeograficheskie rubezhi i metody ikh izucheniya (Paleogeographic Barriers and the Methods of Their Study), Vladivostok: Dal’nevost. Nauch. Tsentr Ross. Akad. Nauk SSSR, 1984, pp. 115–120.

    Google Scholar 

  72. Chereshnev, I.A., Biogeografiya presnovodnykh ryb Dal’nego Vostoka Rossii (Biogeography of Freshwater Fishes of the Russian Far East), Vladivostok: Dal’nauka, 1998.

    Google Scholar 

  73. Parpura, I.Z., On the origin of ichthyofauna of the rivers of northern Primorye, Vopr. Ikhtiol., 1989, vol. 29, no. 3, pp. 506–508.

    Google Scholar 

  74. Nikiforov, S.N., On formation history of the ichthyofauna of inland water bodies in the southern and central parts of the western Sakhalin, Vopr. Ikhtiol., 1999, vol. 39, no. 4, pp. 564–566.

    Google Scholar 

  75. Semenchenko, A.Yu., Primorskaya sima: Populyatsionnaya ekologiya, morfologiya, vosproizvodstvo (Primorye Masu: Population Ecology, Morphology, and Reproduction), Vladivostok: Dal’nevost. Otd. Ross. Akad. Nauk SSSR, 1989.

    Google Scholar 

  76. Salmenkova, E.A., Altukhov, Yu.P., Viktorovskii, R.M., et al., Genetic structure of chum salmon populations that reproduce in rivers of the Far East and the Northeast of the USSR, Zh. Obshch. Biol., 1986, vol. 47, no. 4, pp. 529–548.

    Google Scholar 

  77. Omel’chenko, V.T., Salmenkova, E.A., and Afanas’ev, K.I., Genetic structure of the chum salmon population in Primorye, Genetika (Moscow), 1992, vol. 28, no. 5, pp. 102–113.

    Google Scholar 

  78. Arai, T., Kotake, A., and Morita, K., Evidence of downstream migration of Sakhalin taimen, Hucho perryi, as revealed by Sr: Ca ratios of otolith, Ichthyol. Res., 2004, vol. 51, pp. 377–380.

    Article  Google Scholar 

  79. Arai, T., Effect of salinity on strontium: calcium ratios in the otoliths of Sakhalin taimen, Hucho perryi, Fish. Sci., 2010, vol. 76, pp. 451–455.

    Article  CAS  Google Scholar 

  80. Honda, K., Kagiwada, H., Takahashi, N., and Miyashita, K., Seasonal stream habitat of adult Sakhalin taimen, Parahucho perryi, in the Bekanbeushi River system, eastern Hokkaido, Japan, Ecol. Freshwater Fish, doi: 10.1111/j.1600-0633.2012.00585.x

  81. Altukhov, Yu.P., Salmenkova, E.A., Ryabova, G.D., and Kulikova, N.I., Population genetic differentiation of chum salmon (Oncorhynchus keta (Walb.)), and effectiveness of some acclimatization measures, Biol. Morya, 1980 no. 3, pp. 23–38.

    Google Scholar 

  82. Altukhov, Yu.P., Geneticheskie protsessy v populyatsiyakh (Genetic Processes in Populations), Moscow: Akademkniga, 2003.

    Google Scholar 

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Original Russian Text © L.A. Skurikhina, A.G. Oleinik, A.D. Kukhlevsky, V.V. Malyar, 2013, published in Genetika, 2013, Vol. 49, No. 9, pp. 1065–1078.

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Skurikhina, L.A., Oleinik, A.G., Kukhlevsky, A.D. et al. Intraspecific polymorphism of mtDNA in Sakhalin taimen Parahucho perryi . Russ J Genet 49, 924–936 (2013). https://doi.org/10.1134/S1022795413070132

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