Polar Biology

, Volume 40, Issue 4, pp 777–786 | Cite as

On the origin and phylogenetic position of Arctic charr (Salvelinus alpinus complex, Salmonidae) from Lake Cherechen’ (middle Kolyma River basin): controversial genetic data

  • Alexander G. Osinov
  • Alexander A. Volkov
  • Sergey S. Alekseyev
  • Aleksey A. Sergeev
  • Mikhail V. Oficerov
  • Alexander F. Kirillov
Original Paper


Within the Arctic charr complex (Salvelinus alpinus complex), many different populations and forms with disputable origin and systematic status have been described. Some of them, such as the charr from Lake Cherechen’ (middle Kolyma River basin), combine characters of different phylogenetic groups, representing a possible consequence of former hybridization. The data on 32 allozyme loci and on nucleotide sequences of 501-bp fragments of the mtDNA control region as well as of 899-bp fragments of exon 2 of the RAG1 gene were used for the analysis of the origin of Lake Cherechen’ charr and their phylogenetic relationships with other representatives of the Arctic charr lineage. As was shown previously, the dwarf and large forms of charr from this lake are morphologically similar to other charr populations from the upper Kolyma River, but bear the mtDNA haplotype of northern Dolly Varden Salvelinus malma malma, not of Taranets charr Salvelinus alpinus taranetzi. The analysis of the allozymes and RAG1 gene confirms the affinity of the Lake Cherechen’ charr to the Arctic charr lineage, but it is insufficient to unambiguously attribute them to the Eurasian or Taranets group. The presence of mtDNA of northern Dolly Varden in Lake Cherechen’ Arctic charr and the replacement of their native mtDNA are the result of the introgressive hybridization with S. m. malma. An alternative explanation connected with incomplete lineage sorting seems highly improbable. Our study confirms a postglacial secondary contact of the representatives of different phylogenetic groups of the S. alpinus-S. malma species complex in the Kolyma basin and in the area from Taimyr to Chukotka. It also indicates the need for more thorough analysis of the morphological and genetic diversity of charr from this region as well as caution in taxonomic decisions.


Allozymes Mitochondrial DNA RAG1 gene Arctic charr lineage Hybridization Introgression Systematics 



We thank D. A. Pavlov (Moscow State University) for language editing of the paper and three anonymous reviewers whose suggestions helped to improve and clarify this manuscript. The research was supported by the Russian Foundation for Basic Research (projects nos. 12-04-00171, 14-04-00022).

Supplementary material

300_2016_2000_MOESM1_ESM.pdf (134 kb)
Supplementary material 1 (PDF 134 kb)
300_2016_2000_MOESM2_ESM.pdf (69 kb)
Supplementary material 2 (PDF 68 kb)


  1. Abbott R, Albach D, Ansell S et al (2013) Hybridization and speciation. J Evol Biol 26:229–246CrossRefPubMedGoogle Scholar
  2. Alekseyev SS, Pichugin MYu, Samusenok VP (2000) Diversity of Arctic charrs in meristic characters, their position in the complex of Salvelinus alpinus and the origin of sympatric forms. J Ichthyol 40:279–297Google Scholar
  3. Alekseyev SS, Bajno R, Gordeeva NV, Reist JD, Power M, Kirillov AF, Samusenok VP, Matveevev AN (2009) Phylogeography and sympatric differentiation of the Arctic charr Salvelinus alpinus (L) complex in Siberia as revealed by mtDNA sequence analysis. J Fish Biol 75:368–392CrossRefPubMedGoogle Scholar
  4. Bandelt H-J, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Behnke RJ (1980) A systematic review of the genus Salvelinus. In: Balon EK (ed) Charrs: salmonid fishes of the genus Salvelinus. Dr W Junk Publishers, The Hague, pp 441–479Google Scholar
  6. Behnke RJ (1984) Organizing the diversity of the Arctic charr complex. In: Johnson L, Burns BL (eds) Biology of the Arctic charr. University of Manitoba Press, Winnipeg, pp 3–21Google Scholar
  7. Berg LS (1948) Freshwater fishes of the USSR and adjacent countries. Pt1, 4th edn. USSR Acad Sci, Moscow (in Russian)Google Scholar
  8. Bolnick DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Ann Rev Ecol Evol Syst 38:459–487CrossRefGoogle Scholar
  9. 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 55:573–586CrossRefPubMedGoogle Scholar
  10. Chereshnev IA (1996) Biological diversity of freshwater fish fauna in the Russian North-East. Dalnauka, Vladivostok (in Russian) Google Scholar
  11. Chereshnev IA, Volobuev VV, Shestakov AV, Frolov SV (2002) Salmonoid fishes in Russian North-East. Dalnauka, Vladivostok (in Russian) Google Scholar
  12. Davis BJ (1964) Disc-electrophoresis method and application to human serum proteins. Ann NY Acad Sci 121:404–427CrossRefPubMedGoogle Scholar
  13. Elz AE (2003) A hierarchical analysis of historical processes and phylogeographic patterns in Salvelinus (Pisces: Salmondiae). MSc thesis, University of British Columbia, Department of Zoology, VancouverGoogle Scholar
  14. Felsenstein J (1993) PHYLIP (phylogeny inference package, version 35c). Department of Genetics, SK-50, University of Washington, SeattleGoogle Scholar
  15. Glubokovsky MK, Frolov SV, Efremov VV, Ribnikova IG, Katugin ON (1993) Phylogenetic relations and the systematic of charr’s fishes in the Elgygytgyn lake. In: Bely VF, Chereshnev IA (eds) The nature of the the Elgygygyn lake hollow. FEB Russian Acad Sci, Magadan, pp 149–177 (in Russian) Google Scholar
  16. Gudkov PK (1993) On sympatric forms of charr of the genus Salvelinus from some lakes of the Chukchi Peninsula. Vopr Ikhtiol 33:618–625 (in Russian) Google Scholar
  17. Gudkov PK, Alekseyev SS, Kirillov AF (2003) Morphological and ecological characteristics of resident charrs of the genus Salvelinus from some lakes of the Sea of Okhotsk and Kolyma regions. J Ichthyol 43:613–624Google Scholar
  18. Hindar K, Ryman N, Stahl G (1986) Genetic differentiation among local populations and morphotypes of Arctic charr, Salvelinus alpinus. Biol J Linn Soc 27:269–285CrossRefGoogle Scholar
  19. Hudson AG, Vonlanthen P, Seehausen O (2011) Rapid parallel adaptive radiations from a single hybridogenic ancestral population. Proc R Soc Lond B 278:58–66CrossRefGoogle Scholar
  20. Kaganovskii AG (1955) Charr from the Bering Sea basin. Vopr Ikhtiol 3:54–56 (in Russian) Google Scholar
  21. Kirillov AF, Sivtseva LN, Zhirkov FN, Sveshnikov YuA, Sivtseva LV, Venediktov SYu, Venediktov EYu, Karpov SO (2014) Cyclostomes and fishes of the Kolyma River basin. Young Sci 2:269–277 (in Russian) Google Scholar
  22. McPhail JD (1961) A systematic study of the Salvelinus alpinus complex in North America. J Fish Res Bd Can 18:793–816CrossRefGoogle Scholar
  23. Mina MV (2010) Should ichthyologists discard the concept of ‘polymorphic’ species? In: Pavlov DS, Dgebuadze YuYu, Shatunovskii MI (eds) Aktual’nye problemy sovremennoi ikhtiologii (K 100-letiyu GV Nikol’skogo) (actual problems of modern ichthyology (Dedicated to the 100-year anniversary of GV Nikol’skii). Tovarischestvo nauchnykh izdanii KMK, Moscow, pp 88–95 (in Russian)Google Scholar
  24. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  25. Osinov AG (1999) The Dolly Varden (Salvelinus malma) of Eurasia and the chars of the Kamchatka River basin: data from allozyme analysis. ISACF Inf Ser 7:173–181Google Scholar
  26. Osinov AG (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. J Ichthyol 41:192–208Google Scholar
  27. Osinov AG (2002) Arctic charr Salvelinus alpinus from Transbaikalia and Taimyr: genetic differentiation and origin. J Ichthyol 42:141–151Google Scholar
  28. Osinov AG, Pavlov SD, Maksimov VA (1996) Allozyme variation and genetic differentiation in populations of Arctic char Salvelinus alpinus (L) from the Baltic Sea-Taimyr part of the range. Russ J Genet 32:474–485Google Scholar
  29. Osinov AG, Alekseev SS, Kirillov AF (2003) Arctic Charr Salvelinus alpinus from Lake Ulakhan-Silyan-Kyuel’ (the Yana River basin): biology, morphology, genetics, and phylogeny. J Ichthyol 43:54–68Google Scholar
  30. Osinov AG, Senchukova AL, Mugue NS, Pavlov SD, Chereshnev IA (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. Biol J Linn Soc 116:63–85CrossRefGoogle Scholar
  31. Peacock AC, Bunting SL, Queen KG (1965) Serum protein electrophoresis in acrylamide gel: patterns for normal human subjects. Science 147:1451–1452CrossRefPubMedGoogle Scholar
  32. Pichugin MYu (2009) The development of an artificial hybrid and revealing elements of reproductive isolation between sympatric forms of Dryagin’s char and “pucheglazka” Salvelinus alpinus complex (Salmonidae) from Sobachye Mountain Lake (Taimyr). J Ichthyol 49:236–248CrossRefGoogle Scholar
  33. Politiv DV, Omel’chenko VT, Salmenkova EA, Malinina TV (1998) Genetic differentiation of Arctic and Far Eastern charrs of the genus Salvelinus. Genetika 14:83–92 (in Russian) Google Scholar
  34. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  35. Quenouille B, Bermingham E, Planes S (2004) Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 31:66–88CrossRefPubMedGoogle Scholar
  36. Radchenko OA (2003) Variability of mitochondrial DNA in populations of lake charrs from genus Salvelinus in the Far East and Siberia. J Ichthyol 43:539–547Google Scholar
  37. Radchenko OA (2004) Variability of nucleotide sequences of mitochondrial DNA cytochrome b gene in charrs of the genus Salvelinus. Russ J Genet 40:244–254CrossRefGoogle Scholar
  38. Savvaitova KA (1961) On systematic position of Kamchatka charrs of the genus Salvelinus. Zool Zhurn 10:1696–1704 (in Russian) Google Scholar
  39. Savvaitova KA (1980) Comments to the “Systematic review of the genus Salvelinus”. In: Balon EK (ed) Charrs: salmonid fishes of the genus Salvelinus. Dr W Junk Publishers, The Hague, pp 480–481Google Scholar
  40. Savvaitova KA (1983) Application of biological species concept to the assessment of systematic position of charrs of the genus Salvelinus (Salmonidae). Vopr Ikhtiol 23:883–893 (in Russian) Google Scholar
  41. Savvaitova KA (1989) Arctic charrs: structure of population systems, perspectives of economic use. Agropromizdat, Moscow (in Russian) Google Scholar
  42. Savvaitova KA (1991) On the problem of sympatric forms in charrs of the genus Salvelinus (Salmonidae) from the waters of East Siberia. In: Chereshnev IA, Glubokovsky MK (eds) Biology of the charrs in the Far East. FEB Academy of Sciences of USSR, Vladivostok, pp 5–20 (in Russian) Google Scholar
  43. Savvaitova KA, Maksimov VA (1980) Speciation in charr of the genus Salvelinus (Salmoniformes, Salmonidae) from lakes of Lena delta. Zool Zhurn 59:1820–1830 (in Russian) Google Scholar
  44. Savvaitova KA, Maksimov VA (1991) On sympatric charrs forms of the genus Salvelinus (Salmonidae) from Pegtimelsky Lakes in Chukotka. In: Chereshnev IA, Glubokovsky MK (eds) Biology of the charrs in the Far East. FEB Acad Sci USSR, Vladivostok, pp 37–56 (in Russian) Google Scholar
  45. Savvaitova KA, Volobuev VV (1978) On the systematics of Arctic charrs Salvelinus alpinus complex (Salmoniformes, Salmonidae). Zool Zhurn 57:1534–1543 (in Russian) Google Scholar
  46. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207CrossRefPubMedGoogle Scholar
  47. Shaklee JB, Allendorf FW, Morizot DC, Whitt GS (1990) Gene nomenclature for protein-coding loci in fish. Trans Am Fish Soc 119:2–15CrossRefGoogle Scholar
  48. Shaposhnikova GKh (1971) Comparative morphological description of some species of the genus Salvelinus (Nilsson) Richardson. Trudy Zool Inst AN SSSR 48:4–29 (in Russian) Google Scholar
  49. Shedko SV, Ginatulina LK, Miroshnichenko IL, Nemkova GA (2007) Phylogeography of mitochondrial DNA in South Asian Dolly Varden charr Salvelinus curilus Pallas, 1814 (Salmoniformes, Salmonidae): mediated gene introgression? Russ J Genet 41:165–176CrossRefGoogle Scholar
  50. Shedko SV, Miroshnichenko IL, Nemkova GA (2012) Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of nuclear RAG1 gene. Russ J Genet 48:575–579CrossRefGoogle Scholar
  51. Šlechtová V, Bohlen J, Tan HH (2007) Families of Cobitoidea (Teleostei; Cypriniformes) as revealed from nuclear genetic data and the position of the mysterious genera Barbucca, Psilorhynchus, Serpenticobitis and Vaillantella. Mol Phylogenet Evol 44:1358–1365CrossRefPubMedGoogle Scholar
  52. Sneath PHA, Sokal RR (1973) Numerical taxonomy. Freeman, San FranciscoGoogle Scholar
  53. Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  54. Swofford DL, Selander RB (1989) BIOSYS-1 A PC program for the analysis of allelic variations in population genetics and biochemical systematics. Release 1.7. University of IllinoisGoogle Scholar
  55. Taylor EB, Lowery E, Lilliestrale A, Elz A, Quinn TP (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. J Evol Biol 21:1609–1625CrossRefPubMedGoogle Scholar
  56. Thompson JD, GibsonTJ Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882CrossRefGoogle Scholar
  57. Viktorovsky RM, Glubokovsky MK, Yermolenko LN, Skopets MB (1981) Chars of the genus Salvelinus from Lake El’gygytgyn (Central Chukotka). In: Levanidov VY (ed) Fishes of the ecosystems of the Far East salmon rivers. Dal’nevost NauchTsentr AN SSSR Press, Vladivostok, pp 67–78 (in Russian)Google Scholar
  58. Yamamoto S, Maekawa K, Morita K, Crane PA, Oleinik AG (2014) Phylogeography of a salmonid fish, Dolly Varden Salvelinus malma: multiple glacial refugia in the North Pacific rim. Zool Sci 31:660–670CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alexander G. Osinov
    • 1
  • Alexander A. Volkov
    • 2
  • Sergey S. Alekseyev
    • 3
    • 4
  • Aleksey A. Sergeev
    • 2
  • Mikhail V. Oficerov
    • 5
  • Alexander F. Kirillov
    • 6
  1. 1.Biological FacultyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Russian Federal Research Institute of Fisheries and Oceanography (VNIRO)MoscowRussia
  3. 3.Kolzov Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia
  4. 4.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia
  5. 5.The State Scientific Institute of Irrigation Fish Breeding, Vorovskogo SettlementNoginski District, MoscowRussia
  6. 6.Yakut Department of Federal State Unitary Enterprise “Gosrybcentr”YakutskRussia

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