Abstract
Evolutionary history, systematics and taxonomy of charrs of the genus Salvelinus and especially of the representatives of the S. alpinus–S. malma species complex remain confused that is connected with a substantial ecological and morphological flexibility of this group and with supposed ancient hybridization between some taxa. For the analysis of phylogenetic relationships and introgressive hybridization between the species of the genus Salvelinus including three endemic species from Lake El’gygytgyn and all main representatives of the S. alpinus–S. malma species complex, nucleotide sequences of the mtDNA control region and two nuclear genes (ITS1 and RAG1) were analyzed. The differences in the topologies of individual gene trees, among other reasons, were connected with incomplete lineage sorting and historical introgressive hybridization between certain taxa. Several cases of mtDNA capture by different taxa and phylogenetic groups were proposed. Main phylogenetic groups of the S. alpinus–S. malma species complex were revised. The origin and phylogenetic relationships of southern Dolly Varden from North America were not unambiguously defined. We proposed that introgressive hybridization had an important role in the evolutionary history of charrs, in particular, in the appearance of a high level of morphological, ecological and taxonomical diversity.
Similar content being viewed by others
References
Abbott, R., D. Albach, S. Ansell, J. W. Arntzen, S. J. E. Baird, N. Bierne, J. Boughman, A. Brelsford, C. A. Buerkle, R. Buggs, R. K. Butlin, U. Dieckmann, F. Eroukhmanoff, A. Grill, S. H. Cahan, J. S. Hermansen, G. Hewitt, A. G. Hudson, C. Jiggins, J. Jones, B. Keller, T. Marczewski, J. Mallet, P. Martinez-Rodriguez, M. Most, S. Mullen, R. Nichols, A. W. Nolte, C. Parisod, K. Pfennig, A. M. Rice, M. G. Ritchie, B. Seifert, C. M. Smadja, R. Stelkens, J. M. Szymura, R. Vainola, J. B. W. Wolf & D. Zinner, 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229–246.
Alekseyev, S. S., R. Bajno, N. V. Gordeeva, J. D. Reist, M. Power, A. F. Kirillov, V. P. Samusenok & A. N. Matveev, 2009. Phylogeography and sympatric differentiation of the Arctic charr Salvelinus alpinus (L.) complex in Siberia as revealed by mtDNA sequence analysis. Journal of Fish Biology 75: 368–392.
Behnke, R. J., 1972. The systematics of salmonid fishes of recently glaciated lakes. Journal of the Fisheries Research Board of Canada 29: 639–671.
Behnke, R. J., 1980. A systematic review of the genus Salvelinus. In Balon, E. K. (ed.), Charrs: Salmonid Fishes of the Genus Salvelinus. Dr. W. Junk Publishers, The Hague: 441–481.
Behnke, R. J., 1984. Organizing the diversity of the Arctic charr complex. In Johnson, L. & B. L. Burns (eds), Biology of the Arctic Charr. University of Manitoba Press, Winnipeg: 3–21.
Behnke, R. J., 1989. Interpreting the phylogeny of Salvelinus. Physiology and Ecology Japan, Special 1: 35–48.
Behnke, R. J., 2002. Trout and Salmon of North America. The Free Press, New York.
Berg, L. S., 1948. Freshwater Fishes of the USSR and Adjacent Countries, 4th ed. USSR Academy of Sciences, Moscow.
Bernatchez, L., H. Glemet, C. C. Wilson & R. G. Danzmann, 1995. lntrogression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Canadian Journal of Fisheries and Aquatic Sciences 52: 179–185.
Brunner, P. C., M. R. Douglas, A. Osinov, C. C. Wilson & L. Bernatchez, 2001. Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evolution 55: 573–586.
Cavender, T. M. & S. Kimura, 1989. Cytotaxonomy and interrelationships of Pacific basin Salvelinus. Physiology and Ecology Japan, Special 1: 49–68.
Chereshnev, I. A. & M. B. Skopets, 1990. Salvethymus svetovidovi gen et sp. nova. A new endemic fish of the subfamily Salmoninae from the Lake El’gygytgyn (Central Chukotka). Journal of Ichthyology 30: 87–103.
Chereshnev, I. A., V. V. Volobuev, A. V. Shestakov & S. V. Frolov, 2002. Salmonoid Fishes in Russian North-East. Dalnauka, Vladivostok [in Russian].
Crane, P. A., L. W. Seeb & J. E. Seeb, 1994. Genetic relationships among Salvelinus species inferred from allozyme data. Canadian Journal of Fisheries and Aquatic Sciences 51: 182–197.
Crespi, B. J. & M. J. Fulton, 2004. Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny. Molecular Phylogenetics and Evolution 31: 658–679.
Crete-Lafreniere, A., L. K. Weir & L. Bernatchez, 2012. Framing the Salmonidae family phylogenetic portrait: a more comprehensive picture from increased taxon sampling. PLoS ONE 7: e46662.
Drummond, A. J. & A. Rambaut, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
Durand, E. Y., N. Patterson, D. Reich & M. Slatkin, 2011. Testing for ancient admixture between closely related populations. Molecular Biology and Evolution 28: 2239–2252.
Esin, E. V., E. S. Bocharova, N. S. Mugue & G. N. Markevich, 2017. Occurrence of sympatric charr groups, Salvelinus, Salmonidae, in the lakes of Kamchatka: a legacy of the last glaciations. Journal of Fish Biology 91: 628–644.
Farris, J. S., M. Källersjö, A. B. Kluge & C. Bult, 1995. Testing significans of incongruence. Cladistics 10: 315–319.
Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
Frolov, S. V., 2000. Karyotype Variability and Evolution in Salmonidae. Dalnauka, Vladivostok [in Russian].
Funk, D. J. & K. E. Omland, 2003. Species level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34: 397–423.
Gernhard, T., 2008. The conditioned reconstructed process. Journal of Theoretical Biology 253: 769–778.
Gladenkov, A Yu, A. E. Oleinik, L. Marincovich & K. B. Barinov, 2002. A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology 183: 321–328.
Glubokovsky, M. K., S. V. Frolov, V. V. Efremov, I. G. Ribnikova & O. N. Katugin, 1993. Phylogenetic relations and the systematic of charr`s fishes in the Elgygytgyn lake. In Bely, V. F. & I. A. Chereshnev (eds), The Nature of the the Elgygygyn Lake Hollow. FEB Russian Academy of Sciences, Magadan: 149–177 [In Russian].
Haas, G. R. & J. D. McPhail, 1991. Systematics and distributions of Dolly Varden (Salvelinus malma) and bull trout (Salvelinus confluentus) in North America. Canadian Journal of Fisheries and Aquatic Sciences 48: 2191–2211.
Hamada, M., N. Takasaki, J. D. Reist, A. L. DeCicco, A. Goto & N. Okada, 1998. Detection of the ongoing sorting of ancestrally polymorphic SINEs toward fixation or loss in populations of two species of charr during speciation. Genetics 150: 301–311.
Heath, T. A., S. M. Hedtke & D. M. Hillis, 2008. Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46: 239–257.
Heled, J. & A. J. Drummond, 2010. Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27: 570–580.
Hewitt, G., 1999. Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68: 87–112.
Hewitt, G., 2000. The genetic legacy of the quaternary ice ages. Nature 405: 907–913.
Hewitt, G., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B 358: 183–195.
Huson, D. H. & C. Scornavacca, 2012. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Systematic Biology 61: 1061–1067.
Jobb, G., 2011. TREEFINDER version of March 2011. Munich, Germany. Distributed by the author. http://www.treefinder.de.
Klemetsen, A., 2010. The charr problem revisited: exceptional phenotypic plasticity promotes ecological speciation in postglacial lakes. Freshwater Reviews 3: 49–74.
Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fishes. Kottelat, Cornol and Freyhof, Berlin.
Lanfear, R., B. Calcott, S. Y. W. Ho & S. Guindon, 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695–1701.
Leache, A. D., R. B. Harris, B. Rannala & Z. Yang, 2014. The influence of gene flow on species tree estimation: a simulation study. Systematic Biology 63: 17–30.
Lecaudey, L. A., U. K. Schliewen, A. G. Osinov, E. B. Taylor, L. Bernatchez & S. J. Weiss, 2018. Inferring phylogenetic structure, hybridization and divergence times within Salmoninae (Teleostei: Salmonidae) using RAD-sequencing. Molecular Phylogenetics and Evolution 124: 82–99.
Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformtics 25: 1451–1452.
Maddison, W. P., 1997. Gene trees in species trees. Systematic Biology 46: 523–536.
McPhail, J. D., 1961. A systematic study of the Salvelinus alpinus complex in North America. Journal of the Fisheries Research Board of Canada 18: 793–816.
Moore, J.-S., R. Bajno, J. D. Reist & E. B. Taylor, 2015. Post-glacial recolonization of the North American Arctic by Arctic char (Salvelinus alpinus): Genetic evidence of multiple northern refugia and hybridization between glacial lineages. Journal of Biogeography 42: 2089–2100.
Oleinik, A. G., L. A. Skurikhina & V. A. Brykov, 2015. Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data. Russian Journal of Genetics 51: 55–68.
Osinov, A. G., 2001. Evolutionary relationships between the main taxa of the Salvelinus alpinus-Salvelinus malma complex: results of a comparative analysis of allozyme data from different authors. Journal of Ichthyology 41: 192–208.
Osinov, A. G. & N. S. Mugue, 2008. Variation of the mitochondrial DNA control region in the populations of southern form of Dolly Varden (Salvelinus malma krascheninnikovi) from Sakhalin. Russian Journal of Genetics 44: 1668–1676.
Osinov, A. G. & S. D. Pavlov, 1998. Allozyme variation and genetic divergence between populations of Arctic char and Dolly Varden (Salvelinus alpinus–S. malma complex). Journal of Ichthyology 38: 42–55.
Osinov, A. G. & A. A. Volkov, 2020. On the origin of two species of charrs (Salvelinus, Salmonidae) in Lake Elgygytgyn: data on the ATPase6-NADH4L region of mitochondrial DNA. Journal of Ichthyology 60: 618–625.
Osinov, A. G., S. S. Alekseyev & A. F. Kirillov, 2003. Arctic charr Salvelinus alpinus from Lake Ulakhan–Silyan–Kyuel’ (the Yana River basin): biology, morphology, genetics, and phylogeny. Journal of Ichthyology 43: 54–68.
Osinov, A. G., A. L. Senchukova, N. S. Mugue, S. D. Pavlov & I. A. Chereshnev, 2015. Speciation and genetic divergence of three species of charrs from ancient Lake El’gygytgyn (Chukotka) and their phylogenetic relationships with other representatives of the genus Salvelinus. Biological Journal of the Linnean Society 116: 63–85.
Osinov, A. G., A. A. Volkov, S. S. Alekseyev, A. A. Sergeev, M. V. Oficerov & A. F. Kirillov, 2017. On the origin and phylogenetic position of Arctic charr (Salvelinus alpinus complex, Salmonidae) from Lake Cherechen (middle Kolyma River basin): controversial genetic data. Polar Biology 40: 777–786.
Osinov, A. G., D. A. Pavlov & A. A. Volkov, 2018. On the origin of the lacustrine charr Salvelinus alpinus complex from the Kolyma and Sea of Okhotsk basins. Journal of Ichthyology 58: 353–370.
Patterson, N., P. Moorjani, Y. Luo, S. Mallick, N. Rohland, Y. Zhan, T. Genschoreck, T. Webster & D. Reich, 2012. Ancient admixture in human history. Genetics 192: 1065–1093.
Phillips, R. B. & T. H. Oakley, 1997. Phylogenetic relationships among the Salmoninae based on nuclear and mitochondrial DNA sequences. In Kocher, T. D. & C. A. Stepien (eds), Molecular Systematics of Fishes. Academic Press, San Diego: 145–162.
Phillips, R. B., S. L. Sajdak & M. J. Domanico, 1995. Relationships among charrs based on DNA sequences. Nordic Journal of Freshwater Research 71: 378–391.
Phillips, R. B., L. I. Gidex, K. M. Westrich & A. L. DeCicco, 1999. Combined phylogenetic analysis of ribosomal ITS1 sequences and new chromosome data supports three subgroups of Dolly Varden char (Salvelinus malma). Canadian Journal of Fisheries and Aquatic Sciences 56: 1504–1511.
Pichugin, M Yu, O. F. Gritsenko & A. G. Osinov, 2008. On morphological diversity of southern Dolly Varden trout Salvelinus malma krasheninnikovi from water bodies of Sakhalin. Journal of Ichthyology 48: 367–390.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
Power, G., 2002. Charrs, glaciations and seasonal ice. Environmental Biology of Fishes 64: 17–35.
Quenouille, B., E. Bermingham & S. Planes, 2004. Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 31: 66–88.
Radchenko, O. A., 2005. Variability of Mitochondrial DNA in Chars of the Genus Salvelinus. NESC FEB RAS, Magadan [in Russian].
Rambaut, A. & A. Drummond, 2007. Tracer: MCMC Trace Analysis Tool Version 1.6.0 Computer Program Distributed by the Authors. Department of Zoology, University of Oxford, Oxford, UK.
Redenbach, Z. & E. B. Taylor, 2002. Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America. Evolution 56: 1021–1035.
Reist, J. D. & C. D. Sawatzky, 2010. Diversity and Distribution of Chars, Genus Salvelinus, in Northwestern North America in the Context of Northern Dolly Varden (Salvelinus malma malma (Walbaum 1792)). Canadian Science Advisory Secretariat Research Document 2010/014. www.dfo-mpo.gc.ca/csas/.
Safronov, S. N. & T. V. Zvezdov, 2005. Salvelinus vasiljevae sp. nova – a New Species of Freshwater Chars (Salmonidae, Salmoniformes) from Northwestern Sakhalin. Journal of Ichthyology 45: 700–711.
Savvaitova, K. A., 1989. Arctic Charrs: Structure of Population Systems, Perspectives of Economic Use. Agropromizdat, Moscow [In Russian].
Savvaitova, K. A. & V. V. Volobuev, 1978. On the systematics of Arctic charrs Salvelinus alpinus complex (Salmoniformes, Salmonidae). Zoologicheskii Zhurnal 57: 1534–1543 [In Russian].
Seehausen, O., 2013. Conditions when hybridization might predispose populations for adaptive radiation. Journal of Evolutionary Biology 26: 279–281.
Shafer, A. B. A., C. I. Cullingham, S. D. Cote & D. W. Coltman, 2010. On glaciers and refugia: a decade of study sheeds new light on the phylogeography of northwestern North America. Molecular Ecology 19: 4589–4621.
Shedko, S. V., L. K. Ginatulina, I. L. Miroshnichenko & G. A. Nemkova, 2007. Phylogeography of mitochondrial DNA in South Asian Dolly Varden charr Salvelinus curilus Pallas, 1814 (Salmoniformes, Salmonidae): mediated gene introgression? Russian Journal of Genetics 41: 165–176.
Shedko, S. V., I. L. Miroshnichenko & G. A. Nemkova, 2012. Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of nuclear RAG1 gene. Russian Journal of Genetics 48: 575–579.
Šlechtová, V., J. Bohlen & H. H. Tan, 2007. Families of Cobitoidea (Teleostei; Cypriniformes) as revealed from nuclear genetic data and the position of the mysterious genera Barbucca, Psilorhynchus, Serpenticobitis, and Vaillantella. Molecular Phylogenetics and Evolution 44: 1358–1365.
Swofford, D. L., 2002. PAUP.* Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts.
Taranets, A. Ya., 1936. Freshwater fishes of the basin of North-Western part of Japanese Sea. Trudy of Zoological Institute of AN USSR 4: 483–537 [In Russian].
Taylor, E. B., 2004. Evolution in mixed company. Evolutionary inferences from studies of natural hybridization in Salmonidae. In: Hendry, A. P. & S. Stearns (eds), Evolution Illuminated. Salmon and Their Relatives. Oxford University Press, Oxford: 232–263.
Taylor, E. B., 2016. The Arctic char (Salvelinus alpinus) “complex” in North America revisited. Hydrobiologia 783: 283–293.
Taylor, E. B. & L. May-McNally, 2015. Genetic analysis of Dolly Varden (Salvelinus malma) across its North American range: evidence for a contact zone in southcentral Alaska. Canadian Journal of Fisheries and Aquatic Sciences 72: 1048–1057.
Taylor, E. B., E. Lowery, A. Lilliestrale, A. Elz & T. P. Quinn, 2008. 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. Journal of Evolutionary Biology 21: 1609–1625.
Than, C. & L. Nakhleh, 2009. Species tree inference by minimizing deep coalescences. PLoS Computational Biology 5: e1000501.
Than, C. V. & N. A. Rosebnerg, 2011. Consistency properties of species tree inference by minimizing deep coalescences. Journal of Computational Biology 18: 1–15.
Than, C., D. Ruths & L. Nakhleh, 2008. PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9: 322.
Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24: 4876–4882.
Todesco, M., M. A. Pascual, G. L. Owens, K. L. Ostevik, B. T. Moyers, S. Hubner, S. M. Heredia, M. A. Hahn, C. Caseys, D. G. Bock & L. H. Rieseberg, 2016. Hybridization and extinction. Evolutionary Applications 9: 892–908.
Viktorovsky, R. M., 1978. Mechanisms of speciation in charrs. Nauka, Moscow [In Russian].
Viktorovsky, R. M., M. K. Glubokovsky, L. N. Yermolenko & M. B. Skopets, 1981. Chars of the genus Salvelinus from Lake El’gygytgyn (Central Chukotka). In Fishes of the ecosystems of the Far East salmon rivers. Dal’nevost. Nauchni Tsentr AN SSSR Press, Vladivostok: 67–78 [In Russian].
Wiens, J. J., 2006. Missing data and the design of phylogenetic analyses. Systematic Biology 54: 731–742.
Wilson, C. C. & L. Bernatchez, 1998. The ghost of hybrids past: fixation of Arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush). Molecular Ecology 7: 127–132.
Wilson, C. C. & P. D. N. Hebert, 1993. Natural hybridization between Arctic char (Salvelinus alpinus) and lake trout (S. namaycush) in the Canadian Arctic. Canadian Journal of Fisheries and Aquatic Sciences 50: 2652–2658.
Yu, Y., R. M. Barnett & L. Nakhleh, 2013. Parsimonious inference of hybridization in the presence of incomplete lineage sorting. Systematic Biology 62: 738–751.
Acknowledgements
We thank S. S. Alekseyev, M. Yu. Pichugin, O. A. Radchenko, P. V. Grigorév, L. Bernatchez, A. Costello, E. B. Taylor, U. K. Schliewen, R. Reiter and S. Yamamoto for help in the collection of the material. The research was supported by the Russian Foundation for Basic Research (Project No. 17-04-00063) and phylogenetic analysis was partially funded by the Russian Science Foundation (#19-74-20189 to N.S.M).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Handling editor: Michael Power
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Online Resource 1
Scientific and common names of all taxa included in the analysis and the maps with modern ranges of main species and representatives of two species complexes are given (DOCX 2100 kb)
Online Resource 2
MDC-based species tree of the genus Salvelinus and phylogenetic networks with one and two reticulation nodes are given (DOCX 280 kb)
Online Resource 3
Phylogenetic networks with three reticulation nodes are given (DOCX 28 kb)
Rights and permissions
About this article
Cite this article
Osinov, A.G., Volkov, A.A. & Mugue, N.S. Charrs of the genus Salvelinus (Salmonidae): hybridization, phylogeny and evolution. Hydrobiologia 848, 705–726 (2021). https://doi.org/10.1007/s10750-020-04478-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-020-04478-6