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Molecular Genetic Analysis of the Relationships and Origin of Smelt (Hypomesus, Osmeridae), a New Component of the Fauna of the Barents Sea

  • ANIMAL GENETICS
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Abstract

This study examines the relationships and origin of a population of smelt (genus Hypomesus) that was recently found in the Barents Sea at a significant distance from the western boundary of its geographic range. Genetic analysis clearly identified this species as pond smelt H. olidus and showed its phylogenetic closeness and shared demographic history with H. olidus from the basin of the Bering Sea. Genetic differentiation indices suggest long isolation of populations of the Pacific and Barents Sea basins. The statistical estimates of historical demographic events, coupled with the paleographic data for the Arctic areas of Russia, show that certain populations of H. olidus might have survived in glacial refugia of the Polar Ural region. H. olidus might have passed repeatedly through a bottleneck in past glacial refugia, as well as in the recent time because of the harsh Arctic conditions.

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REFERENCES

  1. Weider, L.J. and Hobæk, A., Phylogeography and Arctic biodiversity: a review, Ann. Zool. Fennici, 2000, vol. 37, pp. 217—231.

    Google Scholar 

  2. Hewitt, G.M., Genetic consequences of climatic oscillations in the Quaternary, Philos. Trans. R. Soc., B, 2004, vol. 359, pp. 183—195. https://doi.org/10.1098/rstb.2003.1388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mecklenburg, C.W., Møller, P.R., and Steinke, D., Biodiversity of arctic marine fishes: taxonomy and zoogeography, Mar. Biodiv., 2011, vol. 41, pp. 109—140. https://doi.org/10.1007/s12526-010-0070-z

    Article  Google Scholar 

  4. Hardy, S.M., Carr, C.M., Hardman, M., et al., Biodiversity and phylogeography of Arctic marine fauna: insights from molecular tools, Mar. Biodiv., 2011, vol. 41, pp. 195—210. https://doi.org/10.1007/s12526-010-0056-x

    Article  Google Scholar 

  5. Layton, K.K.S., Corstorphine, E.A., and Hebert, P.D.N., Exploring Canadian echinoderm diversity through DNA barcodes, PLoS One, 2016, vol. 11, no. 11. e0166118. https://doi.org/10.1371/journal.pone.0166118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Klyukanov, V.A., Genesis, Dispersal, and Evolution of Osmeridae, in Osnovy klassifikatsii i filogenii lososevidnykh ryb (Priciples of Classification and Phylogeny of Salmoniformes), Leningrad: Zool. Inst. Akad. Nauk SSSR, 1977, pp. 13—27.

  7. Lee, D.S., Gilbert, C.R., Hocutt, C.H., et al., Atlas of North American Freshwater Fishes, Raleigh, NC: North Carolina Biological Survey, 1980.

  8. Chereshnev, I.A., Volobuev, V.V., Shestakov, A.V., and Frolov, S.V., Lososevidnye ryby Severo-Vostoka Rossii (Salmonid Fishes in Russian North-East), Vladivostok: Dal’nauka, 2002.

  9. Sawatzky, C.D., Michalak, D., Reist, J.D., et al., Distributions of Freshwater and Anadromous Fishes from the Mainland Northwest Territories, Canada, Can. Manuscr. Rep. Fish. Aquat Sci., 2793, 2007.

  10. Novoselov, A.P., Kondakov, A.V., Gofarov, M.Yu., and Bolotov, I.N., Pond smelt Hypomesus olidus (Osmeridae)—a new species for the fauna of the Barents Sea, J. Ichthyol., 2019, vol. 59, no. 1, pp. 25–30. https://doi.org/10.1134/S0042875219010090.

    Article  Google Scholar 

  11. Skurikhina, L.A., Kukhlevskii, A.D., Zheleznova, K.O., and Kovalev, M.Yu., Analysis of the mitochondrial DNA variation in pond smelt Hypomesus olidus (Osmeridae), Russ. J. Genet., 2012, vol. 48, no. 7, pp. 713—722. https://doi.org/10.1134/S1022795412060142

    Article  CAS  Google Scholar 

  12. 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, no. 5, pp. 730—734.

    Article  CAS  Google Scholar 

  13. 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 

  14. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, New York: Oxford Univ. Press, 2000.

    Google Scholar 

  15. Hudson, R.R., Slatkin, M., and Maddison, W.P., Estimation of levels of gene flow from DNA sequence data, Genetics, 1992, vol. 132, no. 2, pp. 583—589.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., et al., DnaSP 6: DNA sequence polymorphism analysis of large datasets, Mol. Biol. Evol., 2017, vol. 34, pp. 3299—3302.

    Article  CAS  PubMed  Google Scholar 

  17. Cockerham, C.C., Analysis of gene frequencies, Genetics, 1973, vol. 74, pp. 679—700.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  19. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 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. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  21. Rogers, 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.

    CAS  PubMed  Google Scholar 

  22. Excoffier, L., Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model, Mol. Ecol., 2004, vol. 13, pp. 853—864.

    Article  CAS  PubMed  Google Scholar 

  23. Rogers, A., Genetic evidence for a Pleistocene population explosion, Evolution, 1995, vol. 49, pp. 608—615.

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  25. Schneider, S. and Excoffier, L., Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA, Genetics, 1999, vol. 152, pp. 1079—1089.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Smith, G.R., Introgression in fishes: significance for paleontology, cladistics, and evolutionary rates, Syst. Biol., 1992, vol. 41, pp. 41—57.

    Article  Google Scholar 

  27. Ilves, K.L. and Taylor, E.B., Evolutionary and biogeographical patterns within the smelt genus Hypomesus in the North Pacific Ocean, J. Biogeogr., 2008, vol. 35, no. 1, pp. 48—64. https://doi.org/10.1111/j.1365-2699.2007.01782.x

    Article  Google Scholar 

  28. Dodson, J.J., Tremblay, S., Colombani, F., et al., Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus), Mol. Ecol., 2007, vol. 16, no. 23, pp. 5030—5043. https://doi.org/10.1111/j.1365-294X.2007.03559.x

    Article  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  31. 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, pp. 512—526.

    CAS  PubMed  Google Scholar 

  32. Kumar, S., Stecher, G., and Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, pp. 1870—1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Skurikhina, L.A., Kukhlevsky, A.D., and Kovpak, N.E., Relationships of osmerid fishes (Osmeridae) of Russia: divergence of nucleotide sequences of mitochondrial and nuclear genes, Genes Genom., 2013, vol. 35, pp. 529—539. https://doi.org/10.1007/s13258-013-0099-z

    Article  CAS  Google Scholar 

  34. Skurikhina, L.A., Oleinik, A.G., Kukhlevskii, A.D., et al., Genetic differentiation of Pacific smelt Osmerus mordax dentex inferred from the data of mitochondrial DNA analysis, Russ. J. Genet., 2015, vol. 51, no. 12, pp. 1221—1232. https://doi.org/10.1134/S102279541512011X

    Article  CAS  Google Scholar 

  35. Skurikhina, L.A., Oleinik, A.G., and Kovpak, N.E., Mitochondrial DNA variation in Pacific capelin (Mallotus villosus catervarius) from the Sea of Okhotsk, inferred from PCR-RFLP analysis, Russ. J. Genet., 2008, vol. 44, no. 7, pp. 812—820.

    Article  Google Scholar 

  36. Melnikova, M.N., Senchukova, A.L., and Pavlov, S.D., New data on mtDNA variability of pond smelt Hypomesus olidus (Osmeridae) from the Commander Islands in comparison with other populations of the species, Biol. Bull., 2018, vol. 45, no. 1, pp. 11—17. https://doi.org/10.1134/S1062359018010089

    Article  Google Scholar 

  37. Chereshnev, I.A., Shestakov, A.V., and Frolov, S.V., On the systematics of species of the genus Hypomesus (Osmeridae) of Peter the Great Bay, Sea of Japan, Russ. J. Mar. Biol., vol. 27, no. 5, pp. 340—346. https://doi.org/10.1023/A:1012500630605

    Article  Google Scholar 

  38. Ivanova, E.I., About the finding of pond smelt in the European North, Tr. Vsesoyuz. Gidrobiol. O-va., 1952, no. 4, pp. 252—259.

  39. Klyukanov, V.A., Taxonomy and phylogenetic relationships of the genera Osmerus and Hypomesus (Osmeridae) and their dispersion, Zool. Zh., 1975, vol. 54, pp. 590—595.

    Google Scholar 

  40. Bogdanov, V.D., Bogdanova, E.N., Gavrilov, A.L., et al., Bioresursy vodnykh ekosistem Polyarnoro Urala (Biological Resources of Aquatic Ecosystems of the Polar Urals), Yekaterinburg: UrO RAN, 2004.

  41. Mel’nichenko, I.P. and Bogdanov, V.D., Ichthyofauna of Small Rivers on the Ural Coast of Baydaratskaya Bay, Vestn. Astrakh. Gos. Tekh. Uni., Ser. Ryb. Khoz., 2016, no. 1, pp. 30—35.

  42. Bogdanov, V.D., Mel’nichenko, I.P., Kizhevatov, Ya.A., and Bogdanova, E.N., Fish population structure of the Baidaratayakhi River Basin, Vestn. Astrakh. Gos. Tekh. Uni., Ser. Ryb. Khoz., 2017, no. 2, pp. 33—44.

  43. Stewart, J.R., Lister, A.M., Barnes, I., and Dalén, L., Refugia revisited: individualistic responses of species in space and time, Proc. R. Soc. B, 2010, vol. 277, pp. 661—671. https://doi.org/10.1098/rspb.2009.1272

    Article  PubMed  Google Scholar 

  44. Skurikhina, L.A., Oleinik, A.G., Kukhlevsky, A.D., et al., Phylogeography and demographic history of the Pacific smelt Osmerus dentex inferred from mitochondrial DNA variation, Pol. Biol., 2018, vol. 41, pp. 877—896. https://doi.org/10.1007/s00300-018-2250-4

    Article  Google Scholar 

  45. McPhail, J.D. and Lindsey, C.C., Freshwater fishes of Northwestern Canada and Alaska, Fish. Res. Board Canada Bull., 1970, vol. 173.

    Google Scholar 

  46. Kuderskii, L.A., Ways of formation of the northern ichthyofauna elements in the northern European territory of the USSR, in Trudy Gosudarstvennogo Nauchno-Issledovatel’skogo Instituta Ozernogo i Rechnogo Rybnogo Khozyaistva (Proceedings of State Research Institute of Lake and River Fisheries), 1987, issue 258, pp. 102—121.

  47. Svendsen, J.I., Alexanderson, H., Astakhov, V.I., et al., Late Quaternary ice sheet history of northern Eurasia, Quat. Sci. Rev., 2004, vol. 23, pp. 1229—1271. https://doi.org/10.1016/j.quascirev.2003.12.008

    Article  Google Scholar 

  48. Makhrov, A.A. and Laius, D.L., Postglacial immigration of fish and lamprey from the Pacific Ocean to the seas of northern Europe, Sib. Ekol. Zh., 2018, vol. 11, no. 3, pp. 265—279. https://doi.org/10.1134/S1995425518030071

    Article  Google Scholar 

  49. Degraaf, D.A., Aspects of the life history of the pond smelt (Hypomesus olidus) in the Yukon and Northwest Territories, Arctic, 1986, vol. 39, no. 3, pp. 260—263.

    Article  Google Scholar 

  50. Jakobsson, M., Pearce, C., Cronin, T.M., et al., Post-glacial flooding of the Bering Land Bridge dated to 11 cal ka BP based on new geophysical and sediment records, Clim. Past, 2017, vol. 13, pp. 991—1005. https://doi.org/10.5194/cp-13-991-2017

    Article  Google Scholar 

  51. Hughes, A.L.C., Gyllencreutz, R., Lohne, Ø.S., et al., The last Eurasian ice sheets—a chronological database and time-slice reconstruction, DATED-1, Boreas, 2016, vol. 45, pp. 1—45. https://doi.org/10.1111/bor.12142

    Article  Google Scholar 

  52. Svendsen, J.I., Faærseth, L.M.B., Gyllencreutz, R., et al., Glacial and environmental changes over the last 60 000 years in the Polar Ural Mountains, Arctic Russia, inferred from a high-resolution lake record and other observations from adjacent areas, Boreas, 2018. https://doi.org/10.1111/bor.12356

    Article  Google Scholar 

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Funding

The study was supported the “Far East” Program 2018–2020 (project no. 18-4-042) and programs of the Ministry of Education and Science (project № АААА-А19-119011500368-9).

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Authors and Affiliations

  1. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    L. A. Skurikhina, A. G. Oleinik & A. D. Kukhlevsky

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

    A. D. Kukhlevsky

  3. Knipovich Polar Research Institute of Marine Fisheries and Oceanography, Northern Branch, 163002, Arkhangelsk, Russia

    A. P. Novoselov

  4. Laverov Federal Center for Integrated Arctic Research, 163000, Arkhangelsk, Russia

    A. P. Novoselov

  5. State Research Institute of Lake and River Fisheries, 199053, St. Petersburg, Russia

    D. S. Sendek

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  1. L. A. Skurikhina
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  2. A. G. Oleinik
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  3. A. D. Kukhlevsky
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  4. A. P. Novoselov
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  5. D. S. Sendek
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Correspondence to L. A. Skurikhina.

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Translated by A. Lisenkova

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Skurikhina, L.A., Oleinik, A.G., Kukhlevsky, A.D. et al. Molecular Genetic Analysis of the Relationships and Origin of Smelt (Hypomesus, Osmeridae), a New Component of the Fauna of the Barents Sea. Russ J Genet 55, 1082–1092 (2019). https://doi.org/10.1134/S1022795419070135

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