Russian Journal of Genetics

, Volume 51, Issue 1, pp 55–68 | Cite as

Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data

  • A. G. Oleinik
  • L. A. Skurikhina
  • Vl. A. Brykov
Animal Genetics


Charrs of the genus Salvelinus (including Salvethymus) represent a monophyletic group of salmonid fishes that diverged from the common ancestor without subdivision into subgenera. The phylogenesis of the genus is characterized by four cycles of mitochondrial genome divergence. The first one, belonging to the Late Miocene—the border between Miocene and Pliocene (6 to 4 million years ago)—was associated with the consecutive divergence of the S. fontinalis, S. namaycush, S. levanidovi, and S. leucomaenis basal branches. Two divergence events, including separation of the ancestral lineage of Western Pacific group of S. m. krascheninnikovi and the following segregation of the common ancestor into two mitochondrial phyla, happened within the period of 3 to 2 million years ago. The next cycle is attributed to the time interval of about 1 million years ago and includes the divergence of both phyla. In one phylum, a relatively quick isolation of Arctic and Eastern Pacific phylogroups, along with the divergence of the latter phylogroup into S. confluentus and S. m. lordi lineages, took place. At the same time, the second phylum diverged into the S. m. malma and S. alpinus phylogenetic groups. At the final stage (Middle to Late Pleistocene), differentiation of the taxa within the phylogenetic groups took place.


Bootstrap Support Phylogenetic Group Basal Branch Bull Trout White Spotted Charr 
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  1. 1.
    Viktorovskii, R.M., Mekhanizmy vidoobrazovaniya u gol’tsov Kronotskogo ozera (Speciation Mechanisms in Charrs of Kronotskoe Lake), Moscow: Nauka, 1978.Google Scholar
  2. 2.
    Savvaitova, K.A., Arkticheskie gol’tsy (struktura populyatsionnykh sistem, perspektivy khozyaistvennogo ispol’zovaniya) (Arctic Charrs: Structure of Population Systems and Perspectives of Commercial Use), Moscow: Agropromizdat, 1989.Google Scholar
  3. 3.
    Glubokovskii, M.K., Evolyutsionnaya biologiya lososevykh ryb (Evolutionary Biology of Salmonid Fishes), Moscow: Nauka, 1995.Google Scholar
  4. 4.
    Chereshnev, I.A., Volobuev, V.V., Shestakov, A.V., and Frolov, S.V., Lososevidnye ryby Severo-Vostoka Rossii (Salmonoid fishes in Russian North-East), Vladivostok: Dal’nauka, 2002.Google Scholar
  5. 5.
    Grewe, P.M., Billington, N., and Hebert, P.D.N., Phylogenetic relationships among members of Salvelinus inferred from mitochondrial DNA divergence, Can. J. Fish. Aquat. Sci., 1990, vol. 47, no. 5, pp. 984–991.CrossRefGoogle Scholar
  6. 6.
    Phillips, R.B. and Oakley, T.H., Phylogenetic relationships among the Salmoninae based on their nuclear and mitochondrial sequences, Molecular Systematics of Fishes, Kocher, T.D. and Sepien, C.A., Eds., San Diego: Academic, 1997, pp. 145–162.CrossRefGoogle Scholar
  7. 7.
    Brunner, P.C., Douglas, M.R., Osinov, A., et al., Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences, Evolution, 2001, vol. 55, no. 3, pp. 573–586.PubMedCrossRefGoogle Scholar
  8. 8.
    Redenbach, Z. and Taylor, E.B., Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America, Evolution, 2002, vol. 56, no. 5, pp. 1021–1035.PubMedCrossRefGoogle Scholar
  9. 9.
    Elz, A.E., A hierarchical analysis of historical processes and phylogeographic patterns in Salvelinus (Pisces: Salmonidae), MSc Thesis, University of British Columbia, Department of Zoology, Vancouver, 2003.Google Scholar
  10. 10.
    Crespi, B.J. and Fulton, M.J., Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny, Mol. Phylogenet. Evol., 2004, vol. 31, pp. 658–679.PubMedCrossRefGoogle Scholar
  11. 11.
    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.CrossRefGoogle Scholar
  12. 12.
    Oleinik, A.G. and Skurikhina, L.A., Mitochondrial DNA diversity and relationships of endemic charrs of the genus Salvelinus from lake Kronotskoye (Kamchatka Peninsula), Hydrobiologia, 2010, vol. 650, pp. 145–159.CrossRefGoogle Scholar
  13. 13.
    Oleinik, A.G., Skurikhina, L.A., and Brykov, Vl.A., Genetic divergence of mitochondrial DNA in white char Salvelinus albus and northern Dolly Varden char Salvelinus malma malma, Russ. J. Genet., 2010, vol. 46, no. 3, pp. 345–355.CrossRefGoogle Scholar
  14. 14.
    Hubert, N., Hanner, R., Holm, E., et al., Identifying Canadian freshwater fishes through DNA barcodes, PLoS One, 2008, vol. 3, no. 6. e2490Google Scholar
  15. 15.
    Taylor, E.B., Lowery, E., Liliestrale, A., et al., 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.PubMedCrossRefGoogle Scholar
  16. 16.
    Alekseyev, S.S., Bajno, R., Gordeeva, N.V., et al., 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.PubMedCrossRefGoogle Scholar
  17. 17.
    Crête-Lafrenière, A., Weir, L.K., and Bernatchez, L., Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling, PLoS One, 2012, vol. 7, no. 10. e46662PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Bogutskaya, N.G. and Naseka, A.M., Katalog beschelyu-snykh i ryb presnykh i solonovatykh vod Rossii s nomenklaturnymi i taksonomicheskimi kommentariyami (Catalog of Agnatha and the Fishes of Fresh and Brackish Waters of Russia with Nomenclatural and Taxonomic Commentaries), Moscow: KMK, 2004.Google Scholar
  19. 19.
    Ronquist, F. and Huelsenbeck, J.P., MRBAYES 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 2003, vol. 19, no. 12, pp. 1572–1574.PubMedCrossRefGoogle Scholar
  20. 20.
    Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4.0b10, Sunderland: Sinauer Associates, 2002.Google Scholar
  21. 21.
    Felsenstein, J., PHYLIP-Phylogeny Inference Package (Version 3.2), Cladistics, 1989, vol. 5, pp. 164–166.Google Scholar
  22. 22.
    McElroy, D., Moran, P., Bermingham, E., and Kornfield, I., REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data, J. Hered., 1992, vol. 83, pp. 153–158.Google Scholar
  23. 23.
    Nei, M. and Li, W.-H., Mathematical model for studying genetic variation in terms of restriction endonucleases, Proc. Natl. Acad. Sci. U.S.A., 1979, vol. 76, pp. 5269–5273.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Nei, M. and Tajima, F., DNA polymorphism detectable by restriction endonucleases, Genetics, 1981, vol. 97, pp. 145–163.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Nei, M. and Miller, J.C., A simple method for estimating average number of nucleotide substitution within and between populations from restriction date, Genetics, 1990, vol. 125, pp. 873–879.PubMedCentralPubMedGoogle Scholar
  26. 26.
    Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 1980, vol. 16, pp. 111–120.PubMedCrossRefGoogle Scholar
  27. 27.
    Nei, M. and Tajima, F., Maximum likelihood estimation of the number of nucleotide substitutions from restriction site data, Genetics, 1983, vol. 105, pp. 207–217.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Nei, M., Molecular Evolutionary Genetics, New York: Columbia Univ. Press, 1987.Google Scholar
  29. 29.
    Templeton, A.R., Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes, Evolution, 1983, vol. 37, pp. 221–244.CrossRefGoogle Scholar
  30. 30.
    Kishino, H. and Hasegawa, M., Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea, J. Mol. Evol., 1989, vol. 29, pp. 170–179.PubMedCrossRefGoogle Scholar
  31. 31.
    Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, pp. 783–791.CrossRefGoogle Scholar
  32. 32.
    Osinov, A.G. and Lebedev, V.S., Salmonid fishes (Salmonidae, Salmoniformes): the systematic position in the superorder Protacanthopterygii, the main stages of evolution, and molecular dating, J. Ichtyol., 2004, vol. 44, no. 9, pp. 690–715.Google Scholar
  33. 33.
    Smith, G.R., Introgression in fishes: significance for paleontology, cladistics, and evolutionary rates, Syst. Biol., 1992, vol. 41, pp. 41–57.CrossRefGoogle Scholar
  34. 34.
    Brykov, Vl.A., Oleinik, A.G., Polyakova, N.E., et al., Punctuate divergent evolution in fish from the Northern Pacific, Russ. J. Genet., 2010, vol. 46, no. 7, pp. 861–866.CrossRefGoogle Scholar
  35. 35.
    Wilhelm, V., Villegas, J., Miquel, Á. et al., The complete sequence of the mitochondrial genome of the chinook salmon, Oncorhynchus tshawytscha, Biol. Res., 2003, vol. 36, pp. 223–231.PubMedGoogle Scholar
  36. 36.
    Funk, D.J. and Omland, K.E., Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA, Annu. Rev. Ecol. Syst., 2003, vol. 34, pp. 397–423.CrossRefGoogle Scholar
  37. 37.
    Phillips, R.B., Sajdak, S.L., and Domanico, M.J., Relationships among charrs based on DNA sequences, Nordic J. Freshwater Res., 1995, vol. 71, pp. 378–391.Google Scholar
  38. 38.
    Phyllips, R.B., Gudex, L.I., Westrich, K.M., and DeCicco, A.L., Combined phylogenetic analysis of ribosomal ITS1 sequences and new chromosome data supports three subgroups of Dolly Varden char (Salvelinus malma), Can. J. Fish. Aquat. Sci., 1999, vol. 56, pp. 1504–1511.CrossRefGoogle Scholar
  39. 39.
    Radchenko, O.A., Izmenchivost’ mitokhondrial’noi DNK gol’tsov roda Salvelinus (Variation of Mitochondrial DNA in Chars of the Genus Salvelinus), Magadan: Severo-Vostochnyi Nauchnyi Tsentr, Dal’nevostochnoe Otdelenie, Rossiiskaya Akademiya Nauk, 2005.Google Scholar
  40. 40.
    Shubina, E.A., Ponomareva, E.V., and Gritsenko, O.F., Population genetic structure of the char species of the Northern Kuril Islands and the rank of the Dolly Varden char in the system of the genus Salvelinus (Salmonidae: Teleostei), Zh. Obshch. Biol., 2006, vol. 67, no. 4, pp. 280–297.PubMedGoogle Scholar
  41. 41.
    Yamamoto, S., Maekawa, K., Morita, K., et al., Population genetic structure and phylogeography of a salmonid fish, Dolly Varden Salvelinus malma: multiple glacial refugia in the North Pacific rim, in 7th International Charr Symposium: Program and Abstracts of Presentations, Yuzhno-Sakhalinsk, 2012, p. 16.Google Scholar
  42. 42.
    Phillips, R.B., Manley, S.A., and Daniels, T.J., Systematics of the salmonid genus Salvelinus inferred from ribosomal DNA sequences, Can. J. Fish. Aquat. Sci., 1994, vol. 51, suppl. 1, pp. 198–204.CrossRefGoogle Scholar
  43. 43.
    Frolov, S.V., Izmenchivost’ i evolyutsiya kariotipov lososevykh ryb (Karyotype Variation and Evolution in Salmonids), Vladivostok: Dal’nauka, 2000.Google Scholar
  44. 44.
    Wilson, C.C. and Hebert, P.D.N., Phylogeography and postglacial dispersal of lake trout (Salvelinus namaycush) in North America, Can. J. Fish. Aquat. Sci., 1996, vol. 53, pp. 2764–2775.CrossRefGoogle Scholar
  45. 45.
    Taylor, E.B., Redenbach, Z., Costello, A.B., et al., Nested analysis of genetic diversity in northwestern North American char, Dolly Varden (Salvelinus malma) and bull trout (Salvelinus confluentus), Can. J. Fish. Aquat. Sci., 2001, vol. 58, pp. 406–420.CrossRefGoogle Scholar
  46. 46.
    Yamamoto, S., Morita, K., Kitano, S., et al., Phylogeography of white-spotted charr (Salvelinus leucomaenis) inferred from mitochondrial DNA sequences, Zool. Sci., 2004, vol. 21, pp. 229–240.PubMedCrossRefGoogle Scholar
  47. 47.
    Radchenko, O.A., Variability of nucleotide sequences of mitochondrial DNA cytochrome b gene in chars of the genus Salvelinus, Russ. J. Genet., 2004, vol. 40, no. 3, pp. 244–254.CrossRefGoogle Scholar
  48. 48.
    Radchenko, O.A., Salmenkova, E.A., and Omel’chenko, V.T., Variation of cytochrome b gene in sympatric chars from Kronotsky Lake (Kamchatka Oblast), Russ. J. Genet., 2006, vol. 42, no. 2, pp. 172–181.CrossRefGoogle Scholar
  49. 49.
    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.CrossRefGoogle Scholar
  50. 50.
    Ayers, S.D., A review of the species status of the Angayukaksurak charr (Salvelinus anaktuvukensis) of northern Alaska: perspectives from molecular and morphological data, MSc Thesis, University of Alaska Fairbanks, Fairbanks, 2010.Google Scholar
  51. 51.
    Osinov, A.G., The Dolly Varden (Salvelinus malma) of Eurasia and the chars of the Kamchatka river basin: data from allozyme analysis, ISACF Inform. Ser., 1999, no. 7, pp. 173–181.Google Scholar
  52. 52.
    Osinov, A.G., Evolution relationships between the main taxa of the Salvelinus alpinus-S. malma complex: results of comparative analysis of allozyme data of different authors, J. Ichtyol., 2001, vol. 41, no. 2, pp. 167–183.Google Scholar
  53. 53.
    Osinov, A.G., Arctic charr Salvelinus alpinus from Transbaikalia and Taimyr: genetic differentiation and origin, J. Ichtyol., 2002, vol. 42, no. 2, pp. 141–151.Google Scholar
  54. 54.
    Osinov, A.G., Alekseev, S.S., and Kirilov, A.F., Arctic charr Salvelinus alpinus from Lake Ulakhan-Silyan-Kyuel’ (the Yana River basin): biology, morphology, genetics, and phylogeny, J. Ichtyol., 2003, vol. 43, no. 1, pp. 54–67.Google Scholar
  55. 55.
    Shedko, S.V., Miroshnichenko, I.L., and Nemkova, G.A. Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of nuclear RAG 1 gene, Russ. J. Genet., 2012, vol. 48, no. 5, pp. 575–579.CrossRefGoogle Scholar
  56. 56.
    Montgomery, D.R., Coevolution of the Pacific salmon and Pacific Rim topography, Geology, 2000, vol. 28, no. 12, pp. 1107–1110.CrossRefGoogle Scholar
  57. 57.
    Ilves, K.L. and Tailor, E.B., Evolutionary and biogeographical patterns within the smelt genus Hypomesus in the North Pacific Ocean, Biogeogr., 2008, vol. 35, pp. 48–64.Google Scholar
  58. 58.
    Oleinik, A.G., On the mutation rates of the mitochondrial and nuclear genomes of salmonid fishes, Russ. J. Mar. Biol., 2000, vol. 26, no. 6, pp. 432–438.CrossRefGoogle Scholar
  59. 59.
    Behnke, R.J., A systematics review of the genus Salvelinus, in Charrs: Salmonid Fishes of the Genus Salvelinus, Balon, E.K., Ed., The Hague: Junk, 1980, pp. 441–480.Google Scholar
  60. 60.
    Behnke, R.J., Interpreting the phylogeny of Salvelinus, Physiol. Ecol. Jpn. Spec., 1989, vol. 1, pp. 35–48.Google Scholar
  61. 61.
    Westrich, K.M., Konkol, N.R., Matsuoka, M.P., and Phillips, R.B., Interspesific relationships among charrs based on phylogenetic analysis of nuclear growth hormone intron sequences, Environ. Biol. Fishes, 2002, vol. 64, pp. 217–222.CrossRefGoogle Scholar
  62. 62.
    Nelson, J.S., Fishes of the World, Hoboken: Wiley, 2006, 4th ed.Google Scholar
  63. 63.
    Savvaitova, K.A., Taxonomy and biogeography of charrs in the Palearctic, in Charrs: Salmonid Fishes of the Genus Salvelinus, Balon, E.K., Ed., The Hague: Junk, 1980, pp. 281–294.Google Scholar
  64. 64.
    Collins, T.M., Fedrigo, O., and Naylor, G.J.P., Choosing the best genes for the job: the case for stationary genes in genome-scale phylogenies, Syst. Biol., 2005, vol. 54, pp. 493–500.PubMedCrossRefGoogle Scholar
  65. 65.
    Hedtke, S.M., Townsend, T.M., and Hillis, D.M., Resolution of phylogenetic conflict in large data sets by increased taxon sampling, Syst. Biol., 2006, vol. 55, pp. 522–529.PubMedCrossRefGoogle Scholar
  66. 66.
    Felsenstein, J., Cases in which parsimony or compatibility methods will be positively misleading, Syst. Zool., 1978, vol. 27, pp. 401–410.CrossRefGoogle Scholar
  67. 67.
    Anderson, F.E. and Swofford, D.L., Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNA, Mol. Phylogenet. Evol., 2004, vol. 33, pp. 440–451.PubMedCrossRefGoogle Scholar
  68. 68.
    Gatesy, J., DeSalle, R., and Wahlberg, N., How many genes should a systematist sample? Conflicting insights from a phylogenomic matrix characterized by replicated incongruence, Syst. Biol., 2007, vol. 56, no. 2, pp. 355–363.PubMedCrossRefGoogle Scholar
  69. 69.
    Chereshnev, I.A. and Skopets, M.B., Salvethymus svetovidovi gen. et. sp. nova—a new endemic fish of the salmonid (Salmoninae) subfamily from Lake El’gygytgyn (Central Chukotka), Vopr. Ikhtiol., 1990, vol. 30, no. 2, pp. 201–213.Google Scholar
  70. 70.
    Stearley, R.F. and Smith, G.R., Phylogeny of the Pacific trout and salmon (Oncorhynchus) and genera of the family Salmonidae, Trans. Am. Fish. Soc., 1993, vol. 122, no. 1, pp. 1–33.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2015

Authors and Affiliations

  • A. G. Oleinik
    • 1
  • L. A. Skurikhina
    • 1
  • Vl. A. Brykov
    • 1
    • 2
  1. 1.Zhirmunsky Institute of Marine Biology, Far Eastern BranchRussian Academy of SciencesVladivostokRussia
  2. 2.School of Natural SciencesFar Eastern Federal UniversityVladivostokRussia

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