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A comparative analysis of mitochondrial DNA genetic variation and demographic history in populations of even- and odd-year broodline pink salmon, Oncorhynchus gorbuscha (Walbaum, 1792), from Sakhalin Island

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Abstract

To assess genetic variation in pink salmon (Oncorhynchus gorbuscha), the polymorphism of nucleotide sequences of the ND2 and Cytb (mtDNA) genes has been analyzed in 404 individuals of even- and odd-year broodlines from 10 temporal samples collected in different years from one river. The data that earlier indicated a high level of genetic differences between samples of the broodlines spawning in even- and odd-numbered years have been confirmed. Genetic differences between samples of early- and late-run fish was detected in a number of cases. A high probability of purifying selection of the studied genes in both broodlines of pink salmon was found using neutrality tests and models based on likelihood methods and Bayesian approach. A median network of haplotypes based on combined mtDNA sequences for even- and odd-year broodlines have revealed the star-like genealogies and the incomplete “sorting” of haplotypes between them. The analysis of distribution of pairwise nucleotide substitutions, neutrality tests, and Bayesian skyline data support the model of expansion for the population of both pink salmon broodlines that occurred at almost the same time. A study of the history of haplotype divergence inferred from the Bayesian chronogram show the similarity of demographic histories in the populations of both broodlines as a reflection of paleoclimate changes in the region.

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References

  • Altukhov YuP, Salmenkova EA, Omelchenko VT (2000) Salmonid fishes: population biology, genetics and management. Blackwell Sci, Oxford, p 368

    Book  Google Scholar 

  • Beacham TD, McIntosh B, MacConnachie C, Spilsted B, White BA (2012) Population structure of pink salmon (Oncorhynchus gorbuscha) in British Columbia and Washington, determined with microsatellites. Fish Bull 110(2):242–256

    Google Scholar 

  • Brunner PC, Douglas MR, Osinov A, Wilson CC, Bernatchez L (2001) Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evolution 55:573–586

    Article  CAS  PubMed  Google Scholar 

  • Brykov VA, Polyakova NE, Skurikhina LA, Kukhlevsky AD (1996) Geographical and temporal mitochondrial DNA variability in populations of pink salmon. J Fish Biol 48:899–909

    Article  CAS  Google Scholar 

  • Brykov VA, Polyakova NE, Skurikhina LA, Kukhlevsky AD, Kirillova ON, Churikov D, Pudovkin AI, Gharrett AJ (1999) Analysis of mtDNA indicates weak temporal genetic heterogeneity in pink salmon spawning runs in two rivers on Sakhalin Island. J Fish Biol 55:617–635

    Article  CAS  Google Scholar 

  • Brykov VA, Polyakova NE, Podlesnykh AV (2003) Divergence of mitochondrial DNA in populations of sockeye salmon Oncorhynchus nerka Walbaum from Azabach’e Lake (Kamchatka). Rus J Genet 39(12):1432–1437

    Article  CAS  Google Scholar 

  • Churikov D, Gharrett AJ (2002) Comparative phylogeography of the two pink salmon broodlines: an analysis based on a mitochondrial DNA genealogy. Mol Ecol 11:1077–1101

    Article  CAS  PubMed  Google Scholar 

  • Churikov D, Matsuoka M, Luan X, Gray YAK, Brykov VLA, Gharrett AJ (2001) Assessment of concordance among genealogical reconstructions from various mtDNA segments in three species of Pacific salmon (genus Oncorhynchus). Mol Ecol 10:2329–2339

    Article  CAS  PubMed  Google Scholar 

  • Crête-Lafrenière A, Weir LK, Bernatchez L (2012) Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling. PLoS One 7(10):e46662. https://doi.org/10.1371/journal.pone.0046662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1. Mol Biol Evol 29(8):1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gharrett AJ, Joyce J, Smoker WW (2013) Fine-scale temporal adaptation within a salmonid population: mechanism and consequences. Mol Ecol 22(17):4457–4469. https://doi.org/10.1111/mec.12400

    Article  PubMed  Google Scholar 

  • Gilk SE, Wang IA, Hoover CL, Smoker WW, Taylor SG, Gray AK, Gharrett AJ (2004) Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability, and variability in family size. Environ Biol Fish 69:287–297

    Article  Google Scholar 

  • Jacobsen MW, da Fonseca RR, Bernatchez L, Hansen MM (2016) Comparative analysis of complete mitochondrial genomes suggests that relaxed purifying selection is driving high nonsynonymous evolutionary rate of the NADH2 gene in whitefish (Coregonus ssp.). Mol Phylogenet Evol 95:161–170

    Article  CAS  PubMed  Google Scholar 

  • Kaev AM, Rudnev VA (2007) Population dynamics of pink salmon Oncorhynchus gorbuscha (Salmonidae) from the southeastern coast of Sakhalin island. J Ichthyol 47(3):228–240

    Article  Google Scholar 

  • Korotky A, Grebennikova T, Razjigaeva N, Volkov V, Mokhova L, Ganzey L, Bazarova V (1997) Marine terraces of Western Sakhalin Island. Catena 30(10):61–81

    Article  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005) Not so different after all: A comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22(5):1208–1222

    Article  PubMed  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy. Bioinformatics 21(5):676–679

    Article  Google Scholar 

  • Kovach RP, Gharrett AJ, Tallmon DA (2012) Genetic change for earlier migration timing in a pink salmon population. Proc Biol Sci 279(1743):3870–3878. https://doi.org/10.1098/rspb.2012.1158

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the gateway computing environments workshop. New Orleans. LA. 14 Nov 2010. pp 1–8

  • Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30(5):1196-1196 205. https://doi.org/10.1093/molbev/mst030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3(5):418–426

    CAS  PubMed  Google Scholar 

  • Nürnberg D, Tiedemann R (2004) Environmental change in the Sea of Okhotsk during the last 1.1 million years. Paleoceanography 19(4) PA4011. https://doi.org/10.1029/2004PA001023

  • Pavlova A, Gan HM, Lee YP, Austin CM, Gilligan DM, Lintermans M, Sunnucks P (2017) Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish. Heredity 118(5):466–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D (2008) jModelTest. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Quinn TP (1993) A review of homing and straying of wild and hatchery-produced salmon. Fish Res 18:29–44

    Article  Google Scholar 

  • Rambaut A (2014) FigTree v1.4.2, a graphical viewer of phylogenetic. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 20 Mar 2018

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/software/tracer/. Accessed 20 Mar 2018

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Salmenkova EA, Gordeeva NV, Altukhov YuP, Afanas’ev KI, Rubtsova GA, Vasil’eva YuV, Omel’chenko VT (2006) Genetic differentiation of pink salmon Oncorhynchus gorbuscha Walbaum in the Asian part of the range. Rus J Genet 42(10):1148–1163

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor

  • Sato S, Urawa S (2017) Genetic variation of Japanese pink salmon populations inferred from nucleotide sequence analysis of the mitochondrial DNA control region. Environ Biol Fish 100:1355–1372. https://doi.org/10.1007/s10641-017-0648-4

    Article  Google Scholar 

  • Seeb LW, Waples RK, Limborg MT, Warheit KI, Pascal CE, Seeb JE (2014) Parallel signatures of selection in temporally iso- lated lineages of pink salmon. Mol Ecol 23:2473–2485

    Article  CAS  PubMed  Google Scholar 

  • Sevilla RG, Diez A, Noren M, Mouchel O, Jerome M, Verrez-Bagnis V, Van Pelt H, Favre-Krey L, Bautista JM (2007) Primers and polymerase chain reaction conditions for DNA Barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Mol Ecol Notes 7:730–734

    Article  CAS  Google Scholar 

  • Shubin AO, Lisitsyn DV (2018) The reasons for the catastrophic decline in the number of pink salmon in the Sakhalin-Kuril region in 2015–2017 and the role of its artificial breeding.The current state and prospects for the development of Salmon Farm in the Far East of Russia. Materials of the scientific conference (Yuzhno-Sakhalinsk, November 7–8, 2017). Yuzhno-Sakhalinsk: Sakhniro, 164p. http://www.sakhniro.ru/userfiles/conference%207-8.11.2017/materials2017.pdf

  • Silva G, Lima FP, Martel P, Castilho R (2014) Thermal adaptation and clinal mitochondrial DNA variation of European anchovy. Proc Biol Sci 281(1792):20141093. https://doi.org/10.1098/rspb.2014.1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smoker WW, Gharrett AJ, Stekoll MS (1998) Genetic variation of return date in a population of pink salmon: a consequence of fluctuating environment or dispersive selection? Alaska Fish Res Bull 5(1):46–54

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N et al (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6 (2013) Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varnavskaya NV (2006) Genetic differentiation of Pacific salmon populations. Publishing House KamchatNIRO, Petropavlovs-Kamchatsky, p 488

    Google Scholar 

  • Wang K, Shi X, Zou J, Kandasamy S, Gong X, Wu Y, Yan Q (2017) Sediment provenance variations in the southern Okhotsk Sea over the last 180 ka: Evidence from light and heavy minerals. Palaeogeogr Palaeoclimatol Palaeoecol 479:61–70. https://doi.org/10.1016/j.palaeo.2017.04.017

    Article  Google Scholar 

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Acknowledgements

We thank the technical staff of the Sokol Biological Station (Sakhalin, Russia) for their assistance and participation in sampling of spawning pink salmon during many years. The study was supported in part by the Russian Science Foundation (grant no. 14-50-00034).

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Correspondence to Aleksandr V. Podlesnykh.

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This article does not contain any studies with human participants or mammals performed by any of the authors. All the experiments on invertebrate animals and gill-bearing aquatic animals (Pisces) were reviewed and approved by the Ethics Committee of the National Scientific Center of Marine Biology of the Far Eastern Branch of the Russian Academy of Sciences and conducted in agreement with the principles expressed in the Declaration of Helsinki.

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Podlesnykh, A.V., Kukhlevsky, A.D. & Brykov, V.A. A comparative analysis of mitochondrial DNA genetic variation and demographic history in populations of even- and odd-year broodline pink salmon, Oncorhynchus gorbuscha (Walbaum, 1792), from Sakhalin Island. Environ Biol Fish 103, 1553–1564 (2020). https://doi.org/10.1007/s10641-020-01040-0

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