Skip to main content
SpringerLink
Log in

On the origin of endemic stone charr in the Kamchatka River basin

  • CHARR III
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The Kamchatka River basin (Kamchatka Peninsula, Russia) is populated by numerous anadromous and resident forms of charr, Salvelinus, including the endemic stone charr, a specialized predator that inhabits the river and its tributaries along with the Northern Dolly Varden. Nucleotide sequences of the entire gene sequence of cytochrome b and cytochrome c oxidase-1, control region and locus of the lactate dehydrogenase gene (LDH-C1) were used for analysis of stone charr differentiation and its phylogenetic relationships with other representatives of the Bering group (Northern Dolly Varden S. malma malma and white charr S. albus). The ratio of within- to between-population divergence of mtDNA nucleotide sequences was analogous to that previously reported for S. malma malma populations. The genealogy of mtDNA haplotypes and analysis of LDH-C1 gene confirms the affinity of stone charr and white charr to the Northern Dolly Varden phylogenetic group. Two divergent mtDNA lineages have been identified in the Kamchatka River basin, with stone charr and white charr being the main carriers of the haplotypes of a new identified group in this region. Evidence has been obtained for the common origin of stone charr from the Kamchatka River basin and Northern Dolly Varden from the Chukchi Peninsula and Alaska.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Balakirev, E. S., V. A. Parensky, M. Y. Kovalev & F. J. Ayala, 2015. Complete mitochondrial genome of the white char Salvelinus albus (Salmoniformes, Salmonidae). Mitochondrial DNA (Part A) 27: 3753–3754.

    Article  CAS  Google Scholar 

  • Balakirev, E. S., V. A. Parensky, M. Y. Kovalev & F. J. Ayala, 2016a. Complete mitochondrial genome of the stone char Salvelinus kuznetzovi (Salmoniformes, Salmonidae). Mitochondrial DNA (Part B) 1: 287–288.

    Article  Google Scholar 

  • Balakirev, E. S., N. C. Romanov & F. J. Ayala, 2016b. Complete mitochondrial genome of the Northern (Salvelinus malma) and Southern (Salvelinus curilus) Dolly Varden chars (Salmoniformes, Salmonidae). Mitochondrial DNA (Part A) 27: 1016–1017.

    Article  CAS  Google Scholar 

  • Bandelt, H.-J., P. Foster & A. Rohl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Barr, I. D. & O. Solomina, 2014. Pleistocene and Holocene glacier fluctuations upon the Kamchatka Peninsula. Global and Planetary Change 113: 110–120.

    Article  Google Scholar 

  • Bogutskaya, N. G. & A. M. Naseka, 2004. Catalogue of agnathans and fishes of fresh and brackish waters of Russia with comments on nomenclature and taxonomy. KMK Scientific Press, Moscow (in Russian).

    Google Scholar 

  • Brigham-Grette, J., 2001. New perspectives on Beringian quaternary paleogeography, stratigraphy, and glacial history. Quaternary Science Reviews 20: 15–24.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Chereshnev, I. A., 1998. Biogeography of Freshwater Fishes in the Far East of Russia. Dal’nauka Press, Vladivostok (in Russian).

    Google Scholar 

  • Chereshnev, I. A., V. V. Volobuev, A. V. Shestakov & S. V. Frolov, 2002. Salmonoid fishes in Russian North-East. Dal’nauka Press, Vladivostok (in Russian).

    Google Scholar 

  • Crête-Lafrenière, 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doiron, S., L. Bernatchez & P. Blier, 2002. A comparative genomics analysis of the potential adaptative value of Arctic charr mtDNA introgression in brook charr populations (Salvelinus fontinalis Mitchill). Molecular Biology and Evolution 19: 1902–1909.

    Article  CAS  PubMed  Google Scholar 

  • Esin, E. V. & G. N. Markevich, 2017. Charrs of the genus Salvelinus of Asian North Pacific: origin, evolution and modern diversity. Kamchatpress, Moscow (in Russian).

    Google Scholar 

  • Esin, E. V., G. N. Markevich & N. O. Melnik, 2017. Morphological characteristic of the stone charr (Salvelinus, Salmonidae) from the Kamchatka River basin. Proceedings of the Kronotsky Nature Reserve 5: 13–25 (in Russian).

    Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.

    PubMed  Google Scholar 

  • Glubokovskii, M. K., 1977. Taxonomic relationships of chars of the genus Salvelinus in the Basin of the Kamchatka River. The Soviet Journal of Marine Biology 3: 24–35.

    Google Scholar 

  • Glubokovsky, M. K., 1995. Evolutionary biology of salmonid fishes. Nauka, Moscow (in Russian).

    Google Scholar 

  • Hutchison, D. W. & A. R. Templeton, 1999. Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53: 1898–1914.

    Article  PubMed  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMeel, O. M., E. M. Hoey & A. Ferguson, 2001. Partial nucleotide sequences, and routine typing by polymerase chain reaction – restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1*90 and *100 alleles. Molecular Ecology 10: 29–34.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nei, M. & S. Kumar, 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.

    Google Scholar 

  • Oleinik, A. G. & L. A. Skurikhina, 2010. Mitochondrial DNA diversity and relationships of endemic charrs of the genus Salvelinus from lake Kronotskoye (Kamchatka Penisula). Hydrobiologia 650: 145–159.

    Article  CAS  Google Scholar 

  • Oleinik, A. G., L. A. Skurikhina & V. A. Brykov, 2010. Genetic divergence of the Salvelinus albus and Salvelinus malma malma mitochondrial DNA. Russian Journal of Genetics 46: 345–355.

    Article  CAS  Google Scholar 

  • Oleinik, A. G., L. A. Skurikhina & V. A. Brykov, 2011. Population genetic structure of Northern Dolly Varden char Salvelinus malma malma in Asia and North America. Russian Journal of Genetics 47: 1456–1467.

    Article  CAS  Google Scholar 

  • Oleinik, A. G., L. A. Skurikhina, E. I. Bondar & V. A. Brykov, 2014. Phylogeography of northern Dolly Varden Salvelinus malma malma based on analysis of mitochondrial DNA. Journal of Zoological Systematics and Evolutionary Research 52: 293–304.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Oleinik, A. G., L. A. Skurikhina & A. D. Kukhlevsky, 2017a. The lactate dehydrogenase gene LDH-C1, a new molecular marker for phylogenetic analysis of salmonid fishes (Salmoniformes: Salmonidae). Russian Journal of Marine Biology 43: 499–502.

    Article  CAS  Google Scholar 

  • Oleinik, A. G., L. A. Skurikhina, A. D. Kukhlevsky & E. I. Bondar, 2017b. Genetic relationships of Chukchi charr Salvelinus andriashevi and Taranetz charr Salvelinus taranetzi. Russian Journal of Genetics 53: 1137–1145.

    Article  CAS  Google Scholar 

  • Osinov, A. G., 1999. The Dolly Varden (Salvelinus malma) of Eurasia and the chars of the Kamchatka river basin: data from allozyme analysis. International Society of Arctic Char Fanatics Information Series 7: 173–181.

    Google Scholar 

  • Osinov, A. G. & S. D. Pavlov, 1998. Allozyme variation and genetic divergence between populations of Arctic charr and Dolly Varden (Salvelinus alpinus–Salvelinus malma complex). Journal of Ichthyology 38: 42–55.

    Google Scholar 

  • Osinov, A. G., A. L. Senchukova, N. S. Mugue, S. D. Pavlov & I. A. Chereshnev, 2015. Speciation and genetic divergence of three species of charr 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.

    Article  Google Scholar 

  • Pavlov, S. D. & K. A. Savvaitova, 1991. The stone char of the Kamchatka River. International Society of Arctic Char Fanatics Information Series 5: 131–134.

    Google Scholar 

  • Radchenko, O. A., E. A. Salmenkova & V. T. Omel’chenko, 2006. Variation of cytochrome b gene in sympatric chars from Kronotsky Lake (Kamchatka Peninsula). Russian Journal of Genetics 42: 172–181.

    Article  CAS  Google Scholar 

  • Rozas, J., A. Ferrer-Mata, J. C. Sánchez-DelBarrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins & A. Sánchez-Gracia, 2017. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34: 3299–3302.

    Article  CAS  PubMed  Google Scholar 

  • Saitou, N. & M. Nei, 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.

    CAS  PubMed  Google Scholar 

  • Salmenkova, E. A., 2016. Genetic connectivity between sympatric populations of closely related char species, Dolly Varden Salvelinus malma and white char Salvelinus albus. Russian Journal of Genetics 52: 74–78.

    Article  CAS  Google Scholar 

  • Savvaitova, K. A., 1989. Arctic Charrs (Structure of Population Systems, Perspectives of Economic use). Agropromizdat, Moscow (in Russian).

    Google Scholar 

  • Savvaitova, К. A. & V. A. Maksimov, 1970. Stone char from the Kamchatka River basin. Nauchnyye Doklady Vysshey Shkoly. Biological sciences 5: 7–20 (in Russian).

    Google Scholar 

  • Shafer, A. A., C. I. Cullingham, S. D. Côté & D. W. Coltman, 2010. Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Molecular Ecology 19: 4589–4621.

    Article  PubMed  Google Scholar 

  • Slatkin, M. & R. R. Hudson, 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555–562.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    CAS  PubMed  Google Scholar 

  • Taranetz, A. Ya., 1933. Some new freshwater fishes from the Far Eastern region. Doklady Akademii Nauk, SSSR 2: 83–85.

    Google Scholar 

  • Taylor, E. B., 2015. Arctic char (Salvelinus alpinus) “complex” in North America revisited. Hydrobiologia 650: 145–159.

    Google Scholar 

  • Taylor, E. B. & S. 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.

    Article  Google Scholar 

  • Uiblein, F., A. Jagsch, W. Honsig-Erlenburg & S. Weiss, 2001. Status, habitat use, and vulnerability of the European grayling in Austrian waters. Journal of Fish Biology 59 (Supple. A): 223-247.

    Google Scholar 

  • Vasil’ev, V. P., 1985. Evolutionary karyology of fishes. Nauka, Moscow (in Russian).

    Google Scholar 

  • Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360: 1847–1857.

    Article  CAS  Google Scholar 

  • Yamamoto, S., S. Kitano, K. Maekawa, I. Koizumi & K. Morita, 2006. Introgressive hybridization between Dolly Varden Salvelinus malma and white-spotted charr Salvelinus leucomaenis on Hokkaido Island, Japan. Journal of Fish Biology 68: 68–85.

    Article  CAS  Google Scholar 

  • Yamamoto, S., K. Maekawa, K. Morita, P. A. Crane & A. G. Oleinik, 2014. Phylogeography of the salmonid fish, Dolly Varden Salvelinus malma: multiple glacial refugia in the North Pacific Rim. Zoological Science 31: 660–671.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We dedicate this article to the memory of the outstanding ichthyologist, our colleague and friend Igor Alexandrovich Chereshnev. Our deep appreciation is extended to V. A. Parensky (National Scientific Center of Marine Biology (NSCMB), FEB RAS) for providing two specimens of stone charr. We thank our colleagues S. V. Frolov (NSCMB FEB RAS) for providing the charr specimens from lakes Achchen and Nachikinskoe and from the Kamchatka, Paratunka, Raduga rivers, T. V. Malinina (Vavilov Institute of General Genetics, RAS, Moscow) for the specimens from the Taimyr Peninsula, P. K. Gudkov (deceased) for the specimens from Lake Sitasjaure, and P. A. Crane (Conservation Genetics Laboratory, 1011 E. Tudor Rd, Anchorage, Alaska, United States) for the specimens from the Frosty Creek, Kongakut River, and Floods Pond. We are also grateful to Tania Koznova (NSCMB FEB RAS) for her help in manuscript preparation, as well as to three anonymous reviewers for the valuable comments on the manuscript.

Funding

This study was financially supported in part by the Presidium of the Far Eastern Branch, Russian Academy of Sciences (Grant no. 18-4-042).

Author information

Authors and Affiliations

  1. National Scientific Center of Marine Biology FEB RAS (A. V. Zhirmunsky Institute of Marine Biology), Palchevskogo, 17, Vladivostok, Russia, 690041

    Alla G. Oleinik, Lubov A. Skurikhina, Andrey D. Kukhlevsky & Evgeniia I. Bondar

  2. Far Eastern Federal University, Vladivostok, Russia, 690600

    Andrey D. Kukhlevsky & Evgeniia I. Bondar

Authors
  1. Alla G. Oleinik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lubov A. Skurikhina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrey D. Kukhlevsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Evgeniia I. Bondar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alla G. Oleinik.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Guest editors: C. E. Adams, C. R. Bronte, M. J. Hansen, R. Knudsen & M. Power/Charr Biology, Ecology and Management

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

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., Kukhlevsky, A.D. et al. On the origin of endemic stone charr in the Kamchatka River basin. Hydrobiologia 840, 21–33 (2019). https://doi.org/10.1007/s10750-018-3867-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3867-6

Keywords

Search

Navigation