Abstract
In order to extend the geography of genetic studies at the broad circumpolar range of Arctic charr we analyzed sequence variation of mtDNA control region (537–547 b.p.) in 25 populations of the European part of Russia and Siberia. In most of them, haplotypes of the Atlantic or of the Siberia phylogenetic groups were found. The results of phylogenetic analysis indicate low segregation between these groups, for that reason they are considered as two subgroups of a single Eurasian group; the composition and ranges of these subgroups are specified. Charr with haplotypes of the Atlantic subgroup were found in Karelia, at Kola Peninsula, Polar Urals, Novaya Zemlya archipelago, Taimyr; charr with haplotypes of the Atlantic subgroup, in Transbaikalia, in mountainous upper reaches of the Yana and the Indigirka basins and in the lower reaches of the Anabar. Both subgroups reveal weak geographical structuring at large geographic scale. Besides, in the lower Anabar basin Arctic charr bearing a haplotype of the Bering group, which introgressed in their genome from the northern form of Dolly Varden were recorded. Our results evidence a wide-scale post-Pleistocene dispersal of the anadromous form of the Atlantic subgroup charr throughout the Atlantic and Arctic Oceans drainage basins; common origin and close phylogenetic relationships of Arctic charr of the Siberian subgroup from different regions of Siberia and their possible migrations between these regions during the Pleistocene glacial maxima. They also confirm the participation of charr from Beringia in the colonization of Siberian Arctic coasts and indicate that they dispersed further to the west than previously known.
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REFERENCES
Alekseyev, S.S., Buldygerov, V.V., Pichugin, M.Yu., and Samusenok, V.P., Distribution of Arctic charr Salvelinus alpinus (Salmonidae) in Transbaikalia, J. Ichthyol., 1999, vol. 39, no. 1, pp. 43–51.
Alekseyev, S.S., Bajno, R., Gordeeva, N.V., Reist, J.D., Power, M., Kirillov, A.F., Samusenok, V.P., and Matveev, A.N., Phylogeography and sympatric differentiation of the Arctic charr Salvelinus alpinus (L.) complex in Siberia as revealed by mtDNA sequence analysis, J. Fish Biol., 2009, vol. 75, pp. 368–392.
Alekseyev, S.S., Gordeeva, N.V., Samusenok, V.P., Matveev, A.N., Andreev, R.S., Yur’ev, A.L., and Smirina, E.M., Extant and extinct forms of Arctic charr Salvelinus alpinus (L.) complex from the Leprindo lake system (Transbaikalia): differentiation in life history, morphology, and genetics, J. Ichthyol., 2013, vol. 53, no. 10, pp. 792–803.
Amstislavskii, A.Z., Two forms of charr Salvelinus alpinus (L.) from Lake Bol’shoe Schuch’e (Polar Urals), Ekologiya, 1976, no. 2, pp. 86–89.
Behnke, R.J., Organizing the diversity of Arctic charr complex, in Biology of the Arctic Charr, Johnson, L. and Burns, B.L., Eds., Winnipeg: Univ. Manitoba Press, 1984, pp. 3-21.
Berg, L.S., Ryby presnykh vod SSSR i sopredel’nykh stran (Freshwater Fishes of USSR and Adjacent Countries), Moscow: Akad. Nauk SSSR, 1948, part 1.
Brunner, P.C., Douglas, M.R., Osinov, A., Wilson, C.C., and Bernatchez, L., Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences, Evolution, 2001, vol. 55, pp. 573–586.
Esin, E.V. and Markevich, G.N., Evolution of the charrs, genus Salvelinus (Salmonidae). 1. Origins and expansion of the species, J. Ichthyol., 2018, vol. 58, no. 2, pp. 187–203.
Esin, E.V., Bocharova, E., Mugue, N.S., and Markevich, G.N., Occurrence of sympatric charr groups, Salvelinus, Salmonidae, in the lakes of Kamchatka: a legacy of the last glaciations, J. Fish Biol., 2017, vol. 91, no. 2, pp. 628–644.
Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, pp. 783–791.
Johnson, L., Arctic charr, in Charrs. Salmonid Fishes of the Genus Salvelinus, Perspectives in Vertebrate Science Series, Balon, E.K., Ed., Hague: Dr. W. Junk, 1980, pp. 15-98.
Jonsson, B. and Jonsson, N., Polymorphism and speciation in Arctic charr, J. Fish Biol., 2001, vol. 58, pp. 605–638.
Kearse, M., Moir, R., Wilson, A., et al., Generous basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data, Bioinformatics, 2012, vol. 28, no. 12, pp. 1647–1649.
Kirillov, F.N., Ryby Yakutii (Fishes of Yakutia), Moscow: Nauka, 1972.
Klemetsen, A., The most variable vertebrate on Earth, J. Ichthyol., 2013, vol. 53, no. 10, pp. 781–791.
McPhail, J.D., A systematic study of the Salvelinus alpinus complex in North America, J. Fish. Res. Board Can., 1961, vol. 18, pp. 793-816.
Mina, M.V., Microevolution of Fishes: Evolutionary Aspects of Phenetic Diversity, New Delhi: Oxonian Press, 1991.
Moore, J.-S., Bajno, R., Reist, J.D., and Taylor, E.B., Post-glacial recolonization of the North American Arctic by Arctic char (Salvelinus alpinus): genetic evidence of multiple northern refugia and hybridization between glacial lineages, J. Biogeogr., 2015, vol. 42, pp. 2089–2100.
Nei, M., Molecular Evolutionary Genetics, New York: Columbia Univ. Press, 1987.
Nei, M. and Tajima, F., DNA polymorphism detectable by restriction endonucleases, Genetics, 1981, vol. 105, pp. 207–217.
Oleinik, A.G., Molecular evolution of charrs of the genus Salvelinus: phylogenetic and phylogeographic aspects, Doctoral (Biol.) Dissertation, Vladivostok, 2003.
Oleinik, A.G. and Skurikhina, L.A., Genetic divergence of sympatric charrs of the genus Salvelinus from Nachikinskoe Lake (Kamchatka), Russ. J. Genet., 2007, vol. 43, no. 8, pp. 910–917.
Oleinik, A.G. and Skurikhina, L.A., Mitochondrial DNA diversity and relationships of endemic charrs of the genus Salvelinus from lake Kronotskoye (Kamchatka Penisula), Hydrobiologia, 2010, vol. 650, no 1, pp. 145–159.
Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Genetic differentiation of three sympatric charr species from the genus Salvelinus inferred from PCR–RFLP analysis of mitochondrial DNA, Russ. J. Genet., 2003, vol. 39, no. 8, pp. 924–929.
Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Genetic differentiation of Dolly Varden charr (Salvelinus malma) and Taranetz charr (Salvelinus taranetzi) inferred from PCR–RFLP analysis of mitochondrial DNA, Russ. J. Genet., 2004, vol. 40, no. 3, pp. 300–306.
Oleinik, A.G., Skurikhina, L.A., Brykov, V.A., Crane, P.A., and Wenburg, J.K., Differentiation of Dolly Varden char Salvelinus malma from Asia and North America inferred from PCR-RFLP analysis of mitochondrial DNA, Russ. J. Genet., 2005, vol. 41, no. 5, pp. 501–508.
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.
Oleinik, A.G., Skurikhina, L.A., and Chukova, E.I., Phylogeography of southern Asian Dolly Varden char Salvelinus malma krascheninnikovi: genealogical analysis of mitochondrial DNA, Russ. J. Genet., 2010, vol. 46, no. 2, pp. 198–209.
Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Population genetic structure of northern Dolly Varden char Salvelinus malma malma in Asia and North America, Russ. J. Genet., 2011, vol. 47, no. 12, pp. 1456–1467.
Oleinik, A.G., Skurikhina, L.A., Bondar, E.I., and Brykov, V.A., Phylogeography of northern Dolly Varden Salvelinus malma malma (Salmoniformes: Salmonidae) from Asia and North America: an analysis based on the mitochondrial DNA genealogy, J. Ichthyol., 2013, vol. 53, no. 10. pp. 820–832.
Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data, Russ. J. Genet., 2015a, vol. 51, no. 1, pp. 55–68.
Oleinik, A.G., Skurikhina, L.A., and Brykov, V.A., Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data, Russ. J. Genet., 2015b, vol. 51, no. 1, pp. 55–68.
Osinov, A.G., Evolutionary relationships between the main taxa of the Salvelinus alpinus–Salvelinus malma complex: results of a comparative analysis of allozyme data from different authors, J. Ichthyol., 2001, vol. 41, pp. 192–208.
Osinov, A.G, Alekseev, S.S., and Kirillov, A.F., Arctic charr Salvelinus alpinus from lake Ulakhan–Silyan–Kyuel’ (the Yana River basin): biology, morphology, genetics, and phylogeny, J. Ichthyol., 2003, vol. 43, pp. 54–68.
Osinov, A.G., Senchukova, A.L., Mugue, N.S., Pavlov, S.D., and Chereshnev, I.A., Speciation and genetic divergence of three species of charr from ancient Lake El’gygytgyn (Chukotka) and their phylogenetic relationships with other representatives of the genus Salvelinus, Biol. J. Linn. Soc., 2015, vol. 116, pp. 63–85.
Osinov, A.G., Volkov, A.A., Alekseyev, S.S., Sergeev, A.A., Oficerov, M.V., and Kirillov, A.F., On the origin and phylogenetic position of Arctic charr (Salvelinus alpinus complex, Salmonidae) from Lake Cherechen’ (middle Kolyma River basin): controversial genetic data, Polar Biol., 2017, vol. 40, pp. 777–786.
Radchenko, O.A., Variability of mitochondrial DNA in populations of lake charrs from genus Salvelinus in the Far East and Siberia, J. Ichthyol., 2003a, vol. 43, no. 4, pp. 539–547.
Radchenko, O.A., Comparative restriction enzyme analysis of mitochondrial DNA in several populations of lake-resident chars of the genus Salvelinus, Russ. J. Genet., 2003b, vol. 39, no. 1, pp. 87–90.
Radchenko, O.A., Variability of nucleotide sequences of mitochondrial DNA cytochrome b gene in charrs of the genus Salvelinus, Russ. J. Genet., 2004, vol. 40, no. 3. pp. 244–254.
Sambrook, J., Fritsch, E.F. and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab. Press, 1989.
Savvaitova, K.A., Arkticheskie gol’tsy (struktura populyatsionnykh system, perspektivy khozyaistvennogo ispol’zovaniya) (Arctic Charr: Structure of Population Systems and Perspectives of Economic Use), Moscow: Agropromizdat, 1989.
Savvaitova, K.A. and Volobuev, V.V., Systematics of Arctic charrs Salvelinus alpinus complex (Salmoniformes, Salmonidae), Zool. Zh., 1978, vol. 57, no. 10, pp. 1534–1543.
Senchukova, A.L., Mugue, N.S., Pavlov, S.D., and Mel’nikova, M.N., Genetic differentiation in charrs of the genus Salvelinus of the Kronotskoe Lake-river system and their relationships with other charr populations of the Kamchatka peninsula, J. Ichthyol., 2013, vol. 53, no. 10, pp. 840–848.
Senchukova, A.L., Pavlov, S.D., Esin, E.V., and Markevich, G.N., Charrs of the genus Salvelinus from Nachikinskoe Lake (Kamchatka Peninsula) and their position in the phylogenetic system of the S. alpinus–S. malma complex, J. Ichthyol., 2015, vol. 55, no. 1, pp. 97–104.
Shedko, S.V., Ginatulina, L.K., Miroshnichenko, I.L., and Nemkova, G.A., Phylogeography of mitochondrial DNA in South Asian Dolly Varden char Salvelinus curilus Pallas, 1814 (Salmoniformes, Salmonidae): mediated gene introgression? Russ. J. Genet., 2007, vol. 43, no. 2, pp. 165–176.
Soshnina, V.A., Pavlov, S.D., and Zelenina, D.A., Relations of Dolly Varden Salvelinus malma Walbaum from Commander Islands with other charr of the genus Salvelinus according to the results of the study of mtDNA, The XVI Int. Sci. Conf. Dedicated to the 20th Anniversary of Foundation of Nature Parks on Kamchatka “Conservation of Biodiversity of Kamchatka and Coastal Waters,” Abstracts of Papers, Petropavlovsk-Kamchatskii: Kamchatpress, 2015, pp. 340–344.
Taylor, E.B., The Arctic char (Salvelinus alpinus) “complex” in North America revisited, Hydrobiologia, 2016, vol. 783, no 1, pp. 283–293.
Taylor, E.B., Lowery, E., Lilliestrale, A., Elz, A., and Quinn, T.P., Genetic analysis of sympatric char populations in western Alaska: Arctic char (Salvelinus alpinus) and Dolly Varden (Salvelinus malma) are not two sides of the same coin, J . Evol. Biol., 2008, vol. 21, pp. 1609–1625.
Yamamoto, S., Maekawa, K., Morita, K., Crane, P.A., and Oleinik, A.G., Phylogeography of the salmonid fish, Dolly Varden Salvelinus malma: multiple glacial refugia in the North Pacific rim, Zool. Sci., 2014, vol. 31, no 10, pp. 660–670.
ACKNOWLEDGMENTS
The authors thank V.S. Borkicheva (Northern department of Polar Institute of Fisheries and Oceanography), S.A. Ganusevich (Wild Animal Rescue Center), E.V. Esin (Russian Federal Research Institute of Fisheries and Oceanography), G.N. Markevich (Kronotsky Nature Biosphere Preserve), A.A. Makhrov (Institute of Ecology and Evolution, Russian Academy of Sciences (IEE RAS)), E.A. Salmenkova (Institute of General Genetics, Russian Academy of Sciences (IGG RAS)), T.P. Sipko (Institute of Ecology and Evolution, Russian Academy of Sciences) for sharing charr tissue samples, R,S. Andreev, A.N. Maveev, V.P. Samusenok, A.L Yur’ev, I.I. Yur’ev, (Irkutsk State University), D.V. Schepotkin, F.N. Shkil’, (Institute of Developmental Biology, Russian Academy of Sciences (IDB RAS)) for field assistance. The study was funded by Russian Foundation for Basic Research (project no. 18-04-00092), by the Presidium of the Russian Academy of Sciences, program no. 41 “Biodiveristy of natural systems and biological resources of Russia” (Government basic research programs, no. 0112-2018-0025, 0108-2018-00015) and conducted under Government basic research programs of IGG RAS, no. 0112-2016-0002 (NVG), IDB RAS, no. 0108-2018-0007 and IEE RAS, no. 0109-2018-0076 (SSA).
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Gordeeva, N.V., Alekseyev, S.S., Kirillov, A.F. et al. Distribution, Composition and Relationships of Phylogenetic Groups of Arctic Charr Salvelinus alpinus (L.) (Salmoniformes, Salmonidae) in the European part of Russia and in Siberia as Revealed by the Analysis of Nucleotide Sequences of Mitochondrial DNA. J. Ichthyol. 58, 808–818 (2018). https://doi.org/10.1134/S0032945218050089
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DOI: https://doi.org/10.1134/S0032945218050089