The morphological and genetic heterogeneity of sockeye salmon Oncorhynchus nerka (from both the mixed samples and the samples collected in different periods of its mass migration) catched in the mouths of the rivers of west (Ozernaya, Bolshaya, and Palana rivers) and east (Kamchatka River) costs of Kamchatka Peninsula has been analyzed. The stocks of the sockeye salmon inhabiting these river basins (including tributaries and lakes) are the largest in Asia. According to the assessment of the biological parameters and the allele frequencies at 45 loci of single-nucleotide polymorphism at the DNA level, no periodicity in the mass-spawning migration of the sockeye salmon in the rivers of the Kamchatka Peninsula’s western coast was revealed. The analysis of the sockeye salmon’s mixed samples collected from the western Kamchatka Peninsula rivers allowed identifying a group of fishes in the sample taken from the Bolshaya River that was ascertained to the lake form. With respect to the Ozernaya and Palana river samples, the phenotypic and genetic heterogeneity was not revealed. The heterogeneity revealed in the fish sample taken from the Kamchatka River’s mouth can point to a complex spatial-genetic structure of the sockeye salmon in the basin of this lake–river system. The differences between the samples collected during the mass migration through the river’s mainstream indicate the successive approach of fishes to the mouth by the local groups that spawn in the different parts of the river basin.
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Altukhov, Yu.P., Salmenkova, E.A., and Omel’chenko, V.T., Populyatsionnaya genetika lososevykh ryb (Population Genetics of Salmon Fishes), Moscow: Nauka, 1997.
Beacham, T.D., Varnavskaya, N.V., McIntosh, B., and MacConnachie, C., Population structure of sockeye salmon from Russia determined with microsatellite DNA variation, Trans. Am. Fish. Soc., 2006a, vol. 135, pp. 97–109. https://doi.org/10.1577/T05-118.1
Beacham, T.D., McIntosh, B., MacConnachie, C., et al., Pacific Rim population structure of sockeye salmon as determined from microsatellite analysis, Trans. Am. Fish. Soc., 2006b, vol. 135, pp. 174–187. https://doi.org/10.1577/T05-149.1
Benjamini, Y. and Hochberg, Y., Controlling the false discovery rate: a powerful and practical approach to multiple testing, J. R. Stat. Soc., Ser. B, 1995, vol. 57, no. 1, pp. 289–300.
Brykov, Vl.A., Polyakova, N.E., Podlesnykh, A.V., et al., The effect of reproduction biotopes on the genetic differentiation of populations of sockeye salmon Oncorhynchus nerka,Russ. J. Genet., 2005, vol. 41, no. 5, pp. 509–517. https://doi.org/10.1007/s11177-005-0119-4
Bugaev, V.F., Aziatskaya nerka (presnovodnyi period zhizni, struktura lokal’nykh stad, dinamika chislennosti) (Asian Sockeye Salmon (Freshwater Period of Life, Local Stock Structure, and Population Number Dynamics)), Moscow: Kolos, 1995.
Bugaev, V.F., Aziatskaya nerka–2 (biologicheskaya struktura i dinamika chislennosti lokal’nykh stad v kontse XX–nachale XXI vv.)(Asian Sockeye Salmon–2 (Biological Structure and Population Dynamics of Local Stocks in the Late 20th to the Early 21st Century), Petropavlovsk-Kamchatski: Kamchatpress, 2011.
Bugaev, V.F. and Dubynin, V.A., Factors influencing on biological parameters and population dynamics of sockeye salmon Oncorhynchus nerka from the Ozernaya and Kamchatka rivers, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2002, vol. 130, pp. 679–757.
Bugaev, V.F., Milovskaya, L.V., Lepskaya, E.V., et al., The study of sockeye salmon Oncorhynchus nerka of the Palanskogo Lake 1990–2001 (northwestern Kamchatka), Izv. Tikhookean. Inst. Rybovod. Okeanogr., 2002, vol. 130, pp. 777–791.
Bugaev, V.F., Ostroumov, A.G., Nepomnyashchii, K.Yu., and Maslov, A.V., Biological features of sockeye salmon Oncorhynchus nerka from the Bol’shaya River (Western Kamchatka) and factors influencing its biological parameters, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2002b, vol. 130, pp. 758–776.
Burgner, R.L., Life history of sockeye salmon (Oncorhynchus nerka), in Pacific Salmon Life Histories, Groot, C. and Margolis, L., Eds., Vancouver: UBC Press, 1991, pp. 3–117.
Elfstrom, C.M., Smith, C.T., and Seeb, J.E., Thirty-two single nucleotide polymorphism markers for high-throughput genotyping of sockeye salmon, Mol. Ecol. Notes, 2006, vol. 6, no. 4, pp. 1255–1259. https://doi.org/10.1111/j.1471-8286.2006.01507.x
Glubokovskii, M.K., Evolyutsionnaya biologiya lososevykh ryb (Evolutionary Biology of Salmonids), Moscow: Nauka, 1995.
Habicht, C., Seeb, L.W., Myers, K.W., et al., Summer–fall distribution of stocks of immature sockeye salmon in the Bering Sea as revealed by single-nucleotide polymorphisms, Trans. Am. Fish. Soc., 2010, vol. 139, no. 4, pp. 1171–1191 http://www.tandfonline.com/doi/suppl/https://doi.org/10.1577/T09-149.1?scroll=top. 10.1577/T09-149.1
Ivankov, V.N., Ecotops of salmonid fishes, in Morfologiya i sistematika lososevykh ryb (Morphology and Systematics of Salmonid Fishes), Leningrad: Zool. Inst., Akad. Nauk SSSR, 1985, pp. 47–54.
Ivankov, V.N. and Ivankova, E.V., Intraspecific reproductive strategies of Pacific salmons of genus Oncorhynchus: functional resemblance and species differences, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2013, vol. 173, pp. 103–118.
Khrustaleva, A.M., Phylogeography of the Asian sockeye salmon Oncorhynchus nerka according to the variability of mitochondrial loci of single nucleotide polymorphisms: analysis of postglacial settlement of the species on the Asian coast of the Pacific Ocean, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2016, vol. 186, pp. 93–106. https://doi.org/10.26428/1606-9919-2016-186-93-106
Khrustaleva, A.M., Inferring adaptive nature of Major Histocompatibility Complex (MHC) polymorphism from single nucleotide substitutions in Asian sockeye salmon populations: II. Factors determining Onne-DAB gene variability in the Kamchatka river basin, Russ. J. Genet., 2018, vol. 54, no. 11, pp. 1314–1324. https://doi.org/10.1134/S102279541811008X
Khrustaleva, A.M., Gritsenko, O.F., and Klovach, N.V., Single-nucleotide polymorphism in populations of sockeye salmon Oncorhynchus nerka from Kamchatka Peninsula, Russ. J. Genet., 2013, vol. 49, no. 11, pp. 1155–1167. https://doi.org/10.1134/S1022795413110094
Khrustaleva, A.M., Klovach, N.V., Gritsenko, O.F., and Seeb, J.E., Intra- and interpopulation variability of southwestern Kamchatka sockeye salmon Oncorhynchus nerka inferred from the data on single nucleotide polymorphism, Russ. J. Genet., 2014, vol. 50, no. 7, pp. 736–748. https://doi.org/10.1134/S1022795414070096
Khrustaleva, A.M., Klovach, N.V., Vedischeva, E.V., et al., Genetic differentiation of sockeye salmon Oncorhynchus nerka from Kamchatka River basin and the lake–river systems of the west coast of the Bering sea as inferred from data on single nucleotide polymorphism, Russ. J. Genet., 2015, vol. 51, no. 10, pp. 980–991. https://doi.org/10.1134/S1022795415090057
Khrustaleva, A.M., Ponomareva, E.V., Ponomareva, M.V., and Klovach, N.V., DNA single nucleotide polymorphism in populations of the sockeye salmon of Kamchatka, the northwest coast of the Sea of Okhotsk, and Chukotka, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2017, vol. 190, pp. 18–32. https://doi.org/10.26428/1606-9919-2017-190-82-89
Khrustaleva, A.M., Ponomareva, E.V., Ponomareva, M.V., et al., Inferring adaptive nature of Major Histocompatibility Complex (MHC) polymorphism from single nucleotide substitutions in Asian sockeye salmon populations: I. Different forms of selection act in sockeye salmon populations from the Ozernaya and Kamchatka rivers, Russ. J. Genet., 2018, vol. 54, no. 10, pp. 1199–1209. https://doi.org/10.1134/S1022795418100071
Konovalov, S.M., Populyatsionnaya biologiya tikhookeanskikh lososei (Population Biology of Pacific Salmons), Moscow: Nauka, 1980.
Krokhin, E.M. and Krogius, F.V., Description of the Bol’shaya River basin and spawning sites of salmonids, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 1937, vol. 9, pp. 3–156.
Maniatis, T., Fritsch, E.F., and Sambrook, J., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1982.
Nei, M. and Li, W.H., Linkage disequilibrium in subdivided populations, Genetics, 1973, vol. 75, no. 1, pp. 213–219.
Pil’ganchuk, O.A., Shpigal’skaya, N.Yu., Dubynin, V.A., et al., Preliminary results of evaluation of heterogeneity of spawning migration of sockeye salmon from the Ozernaya River, Materialy Vserossiiskoi nauchnoi konferentsii “Vodnye biologicheskie resursy severnoi chasti Tikhogo okeana: sostoyanie, monitoring, upravlenie” (Proc. All-Russ. Sci. Conf. “Water Biological Resources of the Northern Part of Pacific Ocean: State, Monitoring, and Management”), Petropavlovsk-Kamchatski: Kamchat. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2012, pp. 431–438.
Pravdin, I.F., Rukovodstvo po izucheniyu ryb (Manual for Analysis of Fishes), Moscow: Pishchevaya Prom-st’, 1966.
Pritchard, J.K., Stephens, M., and Donnelly, P., Inference of population structure using multilocus genotype data, Genetics, 2000, vol. 155, no. 2, pp. 945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Pustovoit, S.P., Intrapopulation genetic variations and interpopulation differentiation of Asian sockeye salmon Oncorhynchus nerka (Walbaum), Genetika, 1994, vol. 30, no. 1, pp. 101–106.
Pustovoit, S.P., Morphometric study of sockeye salmon Oncorhynchus nerka (Walbaum) from the Palana River (western coast of Kamchatka Peninsula), Vestn. Sev.-Vost. Gos. Univ., 2014, no. 21, pp. 67–72.
Raymond, M. and Rousset, F., GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism, J. Hered., 1995, vol. 86, pp. 248–249.
Seeb, J.E., Pascal, C.E., Ramakrishnan, R., and Seeb, L.W., SNP genotyping by the 5'-nuclease reaction: advances in high throughput genotyping with non-model organisms, in Methods in Molecular Biology, Single Nucleotide Polymorphisms, Komar, A., Ed., New York: Humana, 2009, pp. 277–292. https://doi.org/10.1007/978-1-60327-411-1_18
Semko, R.S., Reserves of salmons and their role for fishery in Western Kamchatka, Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 1954, vol. 41, pp. 3–109.
Smirnov, A.I., Biologiya, razmnozhenie i razvitie tikhookeanskikh lososei (Biology, Reproduction, and Development of Pacific Salmons), Moscow: Mosk. Gos. Univ., 1975.
Smith, C.T., Elfstrom, C.M., Seeb, J.E., and Seeb, L.W., Use of sequence data from rainbow trout and Atlantic salmon for SNP detection in Pacific salmon, Mol. Ecol., 2005, vol. 14, pp. 4193–4203. https://doi.org/10.1111/j.1365-294X.2005.02731.x
Varnavskaya, N.V., Geneticheskaya differentsiatsiya populyatsii tikhookeanskikh lososei (Genetic Differentiation of Pacific Salmon Population), Petropavlovsk-Kamchatski: Kamchat. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2006.
Varnavskaya, N.V., Wood, C.C., and Everett, R., Genetic variation in sockeye salmon (Oncorhynchus nerka) populations of Asia and North America, Can. J. Fish. Aquat. Sci., 1994, vol. 51, suppl. 1, pp. 132–146.
Wood, C.C., Life history variation and population structure in sockeye salmon, Am. Fish. Soc. Symp., 1995, vol. 17, pp. 195–216.
Wood, C.C., Riddell, B.E., and Rutherford, D.T., Alternative juvenile life histories of sock-eye salmon (Oncorhynchus nerka) and their contribution to production in the Stikine River, Northern British Columbia, in Sockeye Salmon (Oncorhynchus nerka): Population Biology and Future Management, Canadian Special Publication of Fisheries and Aquatic Sciences vol. 96, Smith, H.D., et al., Eds., Ottawa: Dep. Fish. Oceans, 1987, pp. 12–24.
Zaporozhets, O.M., Zaporozhets, G.V., and Zorbidi, Zh.Kh., Population dynamics and biological characteristics of Pacific salmons from the Bol’shaya River (Western Kamchatka), Izv. Tikhookean. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2013, vol. 174, pp. 38–68.
Zhivotovsky, L.A., On the methodology of studying population structure using genetic markers (with reference to pink salmon Oncorhynchus gorbuscha), J. Ichthyol., 2013, vol. 53, no. 5, pp. 359–364. https://doi.org/10.1134/S0032945213030144
We are grateful to Dr. J. Seeb (School of Aquatic and Fishery Sciences, University of Washington, Seattle) for his comprehensive assistance and support, the survey management and investment financing, and the provision of methods and using equipment and supplies. We are grateful to the staff of the Ecological Genetics Laboratory, Department of Hydrobiology and Fishery, Washington State University. In addition, we appreciate the data analysis support of M.V. Shitova (Vavilov Institute of General Genetics, Russian Academy of Sciences) and P.K. Afanasiev (All-Russia Research Institute of Fishery and Oceanography).
The survey was supported by the Russian Foundation for Basic Research, grant no. 17-04-00668A.
Conflict of interest. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Translated by O. Zhiryakova
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Khrustaleva, A.M., Klovach, N.V. Morphological and Genetic Heterogeneity of Sockeye Salmon Oncorhynchus nerka (Salmonidae) of Large Lake–River Systems in Eastern and Western Kamchatka. J. Ichthyol. 59, 853–863 (2019). https://doi.org/10.1134/S0032945219060055
- sockeye salmon Oncorhynchus nerka
- mixed samples
- morphological traits
- genetic heterogeneity
- loci of single-nucleotide polymorphism
- sample clusterization and classification