Skip to main content
SpringerLink
Log in

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

  • Animal Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Viktorovskii, R.M., Mekhanizmy vidoobrazovaniya u gol’tsov Kronotskogo ozera (Speciation Mechanisms in Charrs of Kronotskoe Lake), Moscow: Nauka, 1978.

    Google Scholar 

  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. Glubokovskii, M.K., Evolyutsionnaya biologiya lososevykh ryb (Evolutionary Biology of Salmonid Fishes), Moscow: Nauka, 1995.

    Google Scholar 

  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. 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.

    Article  CAS  Google Scholar 

  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.

    Chapter  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  14. Hubert, N., Hanner, R., Holm, E., et al., Identifying Canadian freshwater fishes through DNA barcodes, PLoS One, 2008, vol. 3, no. 6. e2490

    Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. e46662

    Article  PubMed Central  PubMed  Google Scholar 

  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. Ronquist, F. and Huelsenbeck, J.P., MRBAYES 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 2003, vol. 19, no. 12, pp. 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  20. Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4.0b10, Sunderland: Sinauer Associates, 2002.

    Google Scholar 

  21. Felsenstein, J., PHYLIP-Phylogeny Inference Package (Version 3.2), Cladistics, 1989, vol. 5, pp. 164–166.

    Google Scholar 

  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. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Nei, M. and Tajima, F., DNA polymorphism detectable by restriction endonucleases, Genetics, 1981, vol. 97, pp. 145–163.

    CAS  PubMed Central  PubMed  Google Scholar 

  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.

    CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Nei, M., Molecular Evolutionary Genetics, New York: Columbia Univ. Press, 1987.

    Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  31. Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, pp. 783–791.

    Article  Google Scholar 

  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. Smith, G.R., Introgression in fishes: significance for paleontology, cladistics, and evolutionary rates, Syst. Biol., 1992, vol. 41, pp. 41–57.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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. 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.

    Article  Google Scholar 

  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. 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.

    CAS  PubMed  Google Scholar 

  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. 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.

    Article  CAS  Google Scholar 

  43. Frolov, S.V., Izmenchivost’ i evolyutsiya kariotipov lososevykh ryb (Karyotype Variation and Evolution in Salmonids), Vladivostok: Dal’nauka, 2000.

    Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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. 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. 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. 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. 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. 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.

    Article  CAS  Google Scholar 

  56. Montgomery, D.R., Coevolution of the Pacific salmon and Pacific Rim topography, Geology, 2000, vol. 28, no. 12, pp. 1107–1110.

    Article  Google Scholar 

  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. 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.

    Article  Google Scholar 

  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. Behnke, R.J., Interpreting the phylogeny of Salvelinus, Physiol. Ecol. Jpn. Spec., 1989, vol. 1, pp. 35–48.

    Google Scholar 

  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.

    Article  Google Scholar 

  62. Nelson, J.S., Fishes of the World, Hoboken: Wiley, 2006, 4th ed.

    Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  66. Felsenstein, J., Cases in which parsimony or compatibility methods will be positively misleading, Syst. Zool., 1978, vol. 27, pp. 401–410.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. 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.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041, Russia

    A. G. Oleinik, L. A. Skurikhina & Vl. A. Brykov

  2. School of Natural Sciences, Far Eastern Federal University, Vladivostok, 690600, Russia

    Vl. A. Brykov

Authors
  1. A. G. Oleinik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. A. Skurikhina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vl. A. Brykov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Oleinik.

Additional information

Original Russian Text © A.G. Oleinik, L.A. Skurikhina, Vl.A. Brykov, 2015, published in Genetika, 2015, Vol. 51, No. 1, pp. 63–77.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oleinik, A.G., Skurikhina, L.A. & Brykov, V.A. Phylogeny of charrs of the genus Salvelinus based on mitochondrial DNA data. Russ J Genet 51, 55–68 (2015). https://doi.org/10.1134/S1022795415010093

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795415010093

Keywords

Search

Navigation