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Genetic variability in anadromous fishes, chum salmon Oncorhynchus keta (Walbaum, 1792), and Sakhalin taimen Parahucho perryi (Brevoort, 1856) from the Northwestern Pacific as a reflection of paleoclimate oscilations

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Abstract

The genetic variability distribution of two mtDNA segments of chum salmon (Oncorhynchus keta) (Walbaum, 1792) and Sakhalin taimen (Parahucho perryi) (Brevoort, 1856) was examined in populations of the Sea of Japan and the Sea of Okhotsk. The values of haplotype and nucleotide variability in these species are, in general, of the same level. The dating of the divergence time of species haplotypes revealed four evolutionary periods in Sakhalin taimen and three in chum salmon. In the taimen, the first divergence time occurred approximately 430 thousand years (kyr) ago, the second 220 kyr ago, and the third 70 kyr ago. In the chum salmon, the first divergence time corresponds to 220 kyr; the second is approximately 100 kyr ago. In both species, the main portion of presently revealed haplotypes evolved over the past 50–10 kyr. Certain glacioeustatic sea level fluctuations influenced each stage of evolution history of species, contributing to their geographic isolation. Demographic population history research found that the initial stage of population growth in the taimen occurred at the time period of approximately 12 kyr ago and was apparently associated with the end of the Last Glacial Maximum. In the chum salmon, this period began somewhat earlier, 30–35 kyr ago; it has accelerated in the past 10–15 kyr. The last glaciation to a lesser extent impacted the demographics of chum salmon, probably due to the greater eurythermity and to the larger range of this species.

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References

  1. Balanov, A. A., Kukhlevsky, D. A., and Brykov, Vl.A., Sebastes flammeus (Jordan et Starks, 1904), a junior synonym of S. iracundus (Jordan et Starks, 1904), with description of fishes from the southern part of the Sea of Okhotsk, J. Ichthyol., 2004, vol. 44, no. 1, pp. 1–9.

    Google Scholar 

  2. Brykov, Vl.A., and Podlesnykh, A.V., Comparative study of mitochondrial DNA in two greenling species (Hexagrammidae: Pisces) and their hybrids from Peter the Great Bay (Sea of Japan) Russ. J. Genet., 2001, vol. 37, no. 12, pp. 1400–1402.

    Article  CAS  Google Scholar 

  3. Brykov, Vl.A, Polyakova, N.E., and Semina, A.V., Comparative analysis of mitochondrial DNA variation in four species of Far Eastern redfins of the genus Tribolodon (Pisces, Cyprinidae), Russ. J. Genet., 2013, vol. 49, no. 3, pp. 310–319.

    Article  CAS  Google Scholar 

  4. Vasilevsky, A.A., Kamennyi vek ostrova Sakhalin (The Stone Age of the Sakhalin Island), Yuzhno-Sakhalinsk: Sakhalin. kn. izd., 2008.

    Google Scholar 

  5. Gorbachev, V.V., Lapinsky, A.G., Prekoki O.V., and Solovenchuk, L.L., Modeling the dynamics of effective population size of Okhotsk Sea Pollock in the Holocene on the basis of genetic variability in the Nd2 and cytb mtDNA loci, Russ. J. Genet., 2014, vol. 50, no. 7, pp. 763–768.

    Article  CAS  Google Scholar 

  6. Kaplin, P.A. and Selivanov, A.O., Izmeneniya urovnya morei Rossii i razvitie beregov: proshloe, nastoyashchee, budushchee (Sea Level Variation of Seas of Russia and Development of Coasts: Past, Present, and Future), Moscow: GEOS, 1999.

    Google Scholar 

  7. Semenchenko, A.Yu. and Zolotukhin, S.F., The effectiveness of reproduction of the Sakhalin taimen Parahucho perryi in rivers of the Sakhalin Island and a strategy for its protection, in Chteniya pamyati Vladimira Yakovlevicha Levanidova (Vladimir Ya. Levanidov’s Biennial Memorial Meetings), Vladivostok: Dal’nauka, 2011, no. 5, pp. 472–482.

    Google Scholar 

  8. Skurikhina, L.A., Oleinik, A.G., Kukhlevsky, A.D., and Malyar, V.V., Intraspecific polymorphism of mtDNA in Sakhalin taimen Parahucho perryi, Russ. J. Genet., 2013, vol. 49, no. 9, pp. 924–936.

    Article  CAS  Google Scholar 

  9. Shedko, S.V., Miroshnichenko, I.L., and Nemkova, G.A., Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of mtDNA data, Russ. J. Genet., 2013, vol. 49, no. 6, pp. 623–637.

    Article  CAS  Google Scholar 

  10. Shedko, S.V., Miroshnichenko, I.L., Nemkova, G.A., et al., Mitochondrial DNA Sequence Variation, Demographic History, and Population Structure of Amur Sturgeon Acipenser schrenckii Brandt, 1869, Russ. J. Genet., 2015, vol. 51, no. 2, pp. 169–184.

    Article  CAS  Google Scholar 

  11. Alexandrou, M.A., Swartz, B.A., Matzke, N.J., and Oakley, T.H., Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae, Mol. Phyl. Evol., 2013, vol. 69, no. 3, pp. 514–523.

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  14. Brown, W.M., George, M.Jr., and Wilson, A.C., Rapid evolution of animal mitochondrial DNA, Proc. Natl. Acad. Sci. U.S.A., 1979, vol. 76, pp. 1967–1971.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Churikov, D., Matsuoka, M., Luan, X., et al., Assessment of concordance among genealogical reconstructions from various mtDNA segments in three species of Pacific salmon (genus Oncorhynchus), Mol. Ecol., 2001, vol. 19, pp. 2329–2339.

    Article  Google Scholar 

  16. Crâte-Lafrenière, A., Weir, L.K., and Bernatchez, L., Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling, PLoS One, 2012, vol. 7, no. 10, p. e46662.

    Article  Google Scholar 

  17. Darriba, D., Taboada, G.L., Doallo, R., and Posada, D., jModel Test 2: more models, new heuristics and parallel computing, Nat. Meth., 2012, vol. 9, no. 8, p. 772.

    Article  CAS  Google Scholar 

  18. Drummond, A.J., Ho, S.Y.W., Phillips, M.J., and Rambaut, A., Relaxed phylogenetics and dating with confidence, PLoS Biol., 2006, vol. 4, no. 5, p. e88.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Drummond, A.J., Rambaut, A., Shapiro, B., and Pybus, O.G., Bayesian coalescent inference of past population dynamics from molecular sequences, Mol. Biol. Evol., 2005, vol. 22, pp. 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  20. Drummond, A.J., Suchard, M.A., Xie, D., and Rambaut, A., Bayesian phylogenetics with BEAUti and the Beast 1.7, Mol. Biol. Evol., 2012, vol. 29, pp. 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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 

  22. Gharrett, A.J., Gray, A.K., and Brykov, Vl.A., Phylogeographic analysis of mitochondrial DNA variation in Alaskan coho salmon, Oncorhynchus kisutch, Fish. Bull., 2001, vol. 99, pp. 528–544.

    Google Scholar 

  23. Grant, W.S., Problems and cautions with sequence mismatch analysis and bayesian skyline plots to infer historical demography, J. Hered., 2015, vol. 106, no. 4, pp. 333–346.

    Article  PubMed  Google Scholar 

  24. Head, M.J., Pillans, B., and Farquhar, S.A., The Early–Middle Pleistocene transition: characterization and proposed guide for the defining boundary, Episodes, 2008, vol. 31, no. 2, pp. 255–259.

    Google Scholar 

  25. Ho, S.Y.W., Calibrating molecular estimates of substitution rates and divergence times in birds, J. Avian Biol., 2007, vol. 38, no. 4, pp. 409–414.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Kass, R.E. and Raftery, A.E., Bayes factors, J. Am. Stat. Assoc., 1995, vol. 90, no. 430, pp. 773–795.

    Article  Google Scholar 

  28. Korotky, A., Grebennikova, T., Razjigaeva, N., et al., Marine terraces of Western Sakhalin Island, Catena, 1997, vol. 30, no. 1, pp. 61–81.

    Article  Google Scholar 

  29. Librado, P. and Rozas J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, pp. 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  30. Marjoram, P. and Donnelly, P., Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution, Genetics, 1994, vol. 136, no. 2, pp. 673–683.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Mayr, E., Animal Species and Evolution, Cambridge, Mass.: Harvard Univ. Press, 1963.

    Book  Google Scholar 

  32. Miller, K., Mountain, G., Wright, J., and Browning, J., A 180-million-year record of sea level and ice volume variations from continental margin and deep-sea isotopic records, Oceanography, 2011, vol. 24, no. 2, pp. 40–53.

    Article  Google Scholar 

  33. Miller, M.A., Pfeiffer, W., and Schwartz, T., Creating the CIPRES Science Gateway for inference of large phylogenetic trees, Proc. Gateway Computing Environments Workshop, 2010, pp. 1–8.

    Google Scholar 

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

    Google Scholar 

  35. Sevilla, R.G., Diez, A., Noren, M., et al., Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes, Mol. Ecol. Notes, 2007, vol. 7, pp. 730–734.

    Article  CAS  Google Scholar 

  36. Stepien, C.A., Dillon, A.K., and Patterson, A.K., Population genetics, phylogeography, and systematics of the thornyhead rockfish (Sebastolobus) along the deep continental slopes of the North Pacific Ocean, Can. J. Fish. Aquat. Sci., 2000, vol. 57, pp. 1701–1717.

    Article  CAS  Google Scholar 

  37. Suchard, M.A., Weiss, R.E., and Sinsheimer, J.S., Bayesian selection of continuous-time Markov chain evolutionary models, Mol. Biol. Evol., 2001, vol. 18, pp. 1001–1013.

    Article  CAS  PubMed  Google Scholar 

  38. 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, no. 10, pp. 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Templeton, A.R., Routman, E., and Phillips, C.A., Separating population structure from population history: a cladistic analysis of the geographic distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum, Genetics, 1995, vol. 140, pp. 767–782.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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 

  42. Yoon, M., Sato, S., Seeb, J.E., et al., Mitochondrial DNA variation and genetic population structure of chum salmon Oncorhynchus keta around the Pacific Rim, J. Fish Biol., 2008, vol. 73, no. 5, pp. 1256–1266.

    Article  Google Scholar 

  43. Yu, J.N., Azuma, N., Yoon, M., et al., Population genetic structure and phylogeography of masu salmon (Oncorhynchus masou masou) inferred from mitochondrial and microsatellite DNA analyses, Zool. Sci., 2010, vol. 27, no. 5, pp. 375–385.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, ul. Pal’chevskogo 17, Vladivostok, 690041, Russia

    V. V. Malyar & Vl. A. Brykov

  2. Far Eastern Federal University, Vladivostok, 690600, Russia

    V. V. Malyar & Vl. A. Brykov

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  1. V. V. Malyar
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Correspondence to V. V. Malyar.

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Original Russian Text © V.V. Malyar, Vl.A. Brykov, 2016, published in Biologiya Morya.

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Malyar, V.V., Brykov, V.A. Genetic variability in anadromous fishes, chum salmon Oncorhynchus keta (Walbaum, 1792), and Sakhalin taimen Parahucho perryi (Brevoort, 1856) from the Northwestern Pacific as a reflection of paleoclimate oscilations. Russ J Mar Biol 42, 330–340 (2016). https://doi.org/10.1134/S1063074016040076

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