Skip to main content
Log in

Repetitive DNA sequences as an indicator of the level of genetic isolation in fish

  • Molecular Phylogenetics
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Although the functional role is still unknown for most types of nuclear noncoding repetitive sequences, some of them proved to provide adequate phylogenetic and taxonomic markers for studying the genetic relationships of organisms at the species and within-species levels. Several markers were used in this work. First, microsatellite markers were used to examine populations varying in the extent of genetic subdivision in marine and anadromous fish, including the Chilean jack mackerel Trachurus murphyi, anadromous brown trout Salmo trutta, and isolated and anadromous char populations. Locus polymorphism was proportional to the gene flow between populations in all cases. Second, satellite DNA was used to study the phylogenetic relationships within the genera Salmo, Oncorhynchus, Salvelinus, and Coregonus. Genetic distances agreed well with the taxonomic relationships based on morphological traits and various biochemical markers and correlated with the evolutionary ages estimated for the groups by other markers. Third, RAPD PCR with a set of 20-mer primers was performed to study the genus Coregonus and anadromous and isolated populations and species of the genus Salvelinus. The resulting phylogenetic trees may help to resolve some disputable taxonomic issues for the groups. A comparison showed that several RAPD-detected sequences contain conserved fragments of coding sequences and polymorphic repeats (minisatellites) from intergenic regions or introns. The finding point to a nonrandom nature of repetitive DNA divergence and may reflect the evolution of the fish groups examined. Heterochromatic satellite repeats were assumed to contribute to generating a reproductive barrier.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Mayr E. 1963. Animal Species and Evolution. Cambridge, MA: Harvard Univ. Press.

    Book  Google Scholar 

  2. Dobzhansky T. 1937. Genetics and the Origin of Species. New York: Columbia Univ. Press.

    Google Scholar 

  3. Arrighi F.E., Bergendahl J., Mandel M. 1968. Isolation and characterization of DNA from fixed cells and tissues. Exp. Cell Res. 50, 47–53.

    Article  CAS  PubMed  Google Scholar 

  4. Ponomareva E.V., Kuzishchin K.V., Volkov A.A., Gordeeva N.V., Ponomareva M.V., Shubina E.A. 2014. Structure and genetic diversity of small populations of brown trout Salmo trutta in Kandalaksha Bay, the White Sea. J. Ichthyol. 54, 41–53.

    Article  Google Scholar 

  5. Shubina E.A., Ponomareva E.V., Gritzenko O.F. 2006. Population genetic structure of the char species of the Northern Kuril Islands and the rank of the Dolly Varden in the system of the genus Salvelinus (Salmonidae: Teleostei). Zh. Obshch. Biol. 67, 280–298.

    CAS  PubMed  Google Scholar 

  6. Mednikov B.M., Shubina E.A., Mel’nikova M.N., Savvaitova K.A. 1999. The problem of the generic status of Pacific salmon and trout: Genetic taxonomic analysis. J. Ichthyol. 39, 10–17.

    Google Scholar 

  7. Shubina E.A., Ponomareva E.V., Gritsenko O.F. 2007. Genetic structure of the Salvelinus genus chars from reservoirs of the Kuril Islands. Biochemisty (Moscow). 72, 1331–1348.

    Article  CAS  Google Scholar 

  8. Shubina E.A., Ponomareva E.V., Glubokov A.I. 2009. Population genetic structure of walleye pollock Theragra chalcogramma (Gadidae, Pisces) from the Bering Sea and Sea of Okhotsk. Mol. Biol. (Moscow). 43, 855–866.

    Article  CAS  Google Scholar 

  9. Feng F., Lo L.C., Lin Z., Zhu Y., Yue G. H. 2005. Isolation and charactserization of microsatellites in a marine food fish specie, golden trevally Gnathanodon speciosus. Mol. Ecol. Notes. 5, 760–761.

    Article  CAS  Google Scholar 

  10. Fedorov A.N., Grechko V.V., Slobodyanyuk S.Ya., Fedorova L.V., Timokhina G.I. 1992. Taxonomic analysis of DNA repeated sequences. Mol. Biol. (Moscow). 26, 464–469.

    CAS  Google Scholar 

  11. Nei M., Li W.H. 1979. Mathematical model for studying genetic variations in terms of restriction endonucleases. Proc. Natl. Acad. Sci. U. S. A. 76, 5269–5273.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Van de Peer Y., De Wachter R. 1994. TREECON for Windows: A software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Applic. Biosci. 10, 569–570.

    Google Scholar 

  13. Subina E.A., Nikitin M.A., Ponomareva E.V., Gritsenko O.F. 2010. Characterization of molecular markers as evidence of adaptive evolution of Salvelinus alpinus × S. malma complex populations of Kuril Islands. Moscow Univ. Biol. Sci. Bull. 65, 190–192.

    Article  Google Scholar 

  14. Shubina E.A., Nikitin M.A., Ponomareva E.V., Goryunov D.V., Gritsenko O.F. 2013. Comparative study of genome divergence in Salmonids with various rates of genetic isolation. Int. J. Genomics. 2013, ID 629543.

    Google Scholar 

  15. Abaunza P., Murta A.G., Campbell N., Cimmaruta R., Comesana A.S., Dahle G., Garcýa Santamarýa M.T., Gordo L.S., Iversen S.A., MacKenzie K., Magoulas A., Mattiucci S., Molloy J., Nascetti G., Pinto A.L., Quinta R., Ramos P., Sanjuan A., Santos A.T., Stransky C., Zimmermann C. 2008. Stock identity of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean Sea: Integrating the results from different stock identification approaches. Fisheries Res. 89, 196–209.

    Article  Google Scholar 

  16. Karaiskou N., Triantafyllidis A., Triantafyllidis C. 2004. Shallow genetic structure of three species of the genus Trachurus in European waters. Mar. Ecol. Prog. Ser. 281, 193–205.

    Article  Google Scholar 

  17. Stepien C.A., Rosenblatt R.H. 1996. Genetic divergence in antitropical pelagic marine fishes (Trachurus, Merluccius, and Scomber) between North and South America. Copeia. 3, 586–598.

    Article  Google Scholar 

  18. Vasil’eva E., Stygar V. 2000. Salvelinus gritzenkoi, a new species of char from the North Kuril Islands (Salmonidae, Salmoniformes). Folia Zool. 49, 317–320.

    Google Scholar 

  19. Grechko V.V., Fedorova L.V., Fedorov A.N., Slobodyanyuk S.Ya., Ryabinin D.M., Melnikova M.N., Bannikova A.A., Lomov A.A., Sheremet’eva V.A., Gorshkov V.A., Sevostyanova G.A., Semenova S.K., Riskov A.P., Mednikov B.M., Darevskii I.S. 1997. Restiction endonuclease analysis of highly repeated DNA sequences sheds light on genetic relatedness of lower taxa of animals. Mol. Biol. (Moscow). 31, 202–209.)

    CAS  Google Scholar 

  20. Roudykh I.A., Grechko V.V., Ciobanu D.G., Kramerov D.A., Darevskii I.S. 2002. Variability of restriction sites in satellite DNA as a molecular basis of taxonoprint method: Evidence from the study of Caucasian rock lizards. Russ. J. Genet. 38, 937–941.

    Article  CAS  Google Scholar 

  21. Gray K.M., White J.W., Costanzi C., Gillespie D., Schroeder W.T., Calabretta B., Saunders G.F. 1985. Recent amplification of an alpha satellite DNA in humans. Nucleic Acids Res. 13, 521–535.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Jeffreys A.J., Wilson V., Thein S.L. 1985. Hypervariable’ minisatellite’ regions in human DNA. Nature. 314, 67–73.

    Article  CAS  PubMed  Google Scholar 

  23. Elder J.F., Turner B.J. 1994. Concerted evolution at the population level: Pupfish HindIII satellite DNA sequences. Proc. Natl. Acad. Sci. U. S. A. 91, 994–998.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Dover G.A. 1982. Molecular drive: A cohesive mode of species evolution. Nature. 299, 111–117.

    Article  CAS  PubMed  Google Scholar 

  25. Ohta T., Dover G.A. 1984. The cohesive population genetics of molecular drive. Genetics. 108, 501–521.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Elder J.F., Turner B.J. 1995. Concerted evolution of repetitive DNA sequences in eukaryotes. Quart. Rev. Biol. 70, 297–320.

    Article  CAS  PubMed  Google Scholar 

  27. Mednikov B.M., Bannikova A.A., Lomov A.A., Melnikova M.N., Shubina E.A. 1995. Restriction endonuclease analysis of repeated nuclear DNA. Species criterion and mechanisms of speciation. Mol. Biol. (Moscow). 29, 778–786.

    Google Scholar 

  28. Smith G.R., Stearley R.F. 1989. The classification and scientific names of rainbow and cutthroat trouts. Fisheries. 14, 4–10.

    Article  Google Scholar 

  29. Bernatchez L., Dodson J.J. 1990. Allopatric origin of sympatric populations of Lake Whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis. Evolution. 4, 1263–1271.

    Article  Google Scholar 

  30. Todd T.N., Smith G.R. 1992. A review of differentiation in great Lakes ciscoes. Pol. Arch. Hydrobiol. 39, 261–267.

    Google Scholar 

  31. Savvaitova K.A. 1995. Patterns of diversity and processes of speciation in Arctic Char. Nord J. Freshw Res. 71, 81–91.

    Google Scholar 

  32. Chereshnev I.A., Skopets M.B. 1990. Salvethymus svetovidovi gen. et sp. nova, a new endemic fish from subfamily Salmonidae from Lake El’gygytgyn (the Central Chukotka). J. Ichthyol. 30, 201–213.

    Google Scholar 

  33. Behnke R.J. 1972. The systematics of salmonid fishes of recently glaciated lakes. J. Fish Res. Board Can. 29, 639–671.

    Article  Google Scholar 

  34. Osinov A.G., Lebedev V.S. 2004. Salmonid fishes (Salmonidae, Salmoniformes): The systematic position in the superorder Protacanthopterygii-the main stages of evolution, and molecular dating. J. Ichthyol. 44, 690–715.

    Google Scholar 

  35. Svardson G. 1979. Speciation of Scandinavian Coregonus. Rep. Inst. Freshw. Res. Drottningholm. 57, 1–95.

    Google Scholar 

  36. Todd T.N. 1981. Allelic variability in species and stocks of Lake Superior ciscoes (Coregoninae). Can. J. Fish. Aquat. Sci. 38, 1808–1813.

    Article  Google Scholar 

  37. Svärdson G. 1970. Significance of introgression in coregonid evolution. In: Biology of Coregonid Fishes. Eds. Lindsey C.C., Woods C.S. Winnipeg, MB: Univ. of Manitoba Press, pp. 33–59.

    Google Scholar 

  38. Ermolenko L.N. 1992. Genetic divergence in the family Coregonidae. Pol. Arch. Hydrobiol. 39, 533–539.

    Google Scholar 

  39. Xu S. 2000. Phylogenetic analysis under reticulate evolution. Mol. Biol. Evol. 17, 897–907.

    Article  CAS  PubMed  Google Scholar 

  40. Svardson G. 1998. Postglacial dispersal and reticulate evolution of Nordic Coregonids. Nord. J. Freshw. Res. 74, 3–32.

    Google Scholar 

  41. Politov D.V., Baldina S.N., Gordon N.Yu. 2010. Modes of speciation in Palearctic Coregonids. Proc. 5th Int. Vereschagin Baikal Conference. Irkutsk, pp. 41–42.

    Google Scholar 

  42. Welsh J., McClelland M. 1991. Genomic fingerprinting using arbitrarily primed PCR and a matrix of pairwise combinations of primers. Nucleic Acids Res. 19, 5275–5279.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Berst A.H., Emery A.R., Spangler G.R. 1981. Reproductive behavior of hybrid charr (Salvelinus fontinalis × S. namaycush). Can. J. Fish Aquat. Sci. 38, 432–440.

    Article  Google Scholar 

  44. Coyne J.A., Orr H.A. 1998. The evolutionary genetics of speciation. Phil. Trans. R. Soc. London, B. 353, 287–305.

    Article  CAS  Google Scholar 

  45. Orr H.A. 2001. The genetics of species differences. Trends Ecol. Evol. 16, 343–350.

    Article  Google Scholar 

  46. Shapiro J.A., von Sternberg R. 2005. Why repetitive DNA is essential to genome function. Biol. Rev. 80, 1–24.

    Article  Google Scholar 

  47. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. 2002. The Molecular Biology of the Cell, 4th ed. New York: Taylor & Francis.

    Google Scholar 

  48. Albanese V., Biguet N.F., Kiefer H., Bayard E., Mallet J., Meloni R. 2001. Quantative effects on gene silencing by allelic variation at a tetranucleotide microsatellite. Hum. Mol. Genet. 10, 1785–1792.

    Article  CAS  PubMed  Google Scholar 

  49. Lewontin R.C. 1972. The apportionment of human diversity. J. Evol. Biol. 6, 381–398.

    Google Scholar 

  50. Grechko V.V. 2011. Repeated DNA sequences as an engine of biological diversification. Mol. Biol. (Moscow). 45, 704–727.

    Article  CAS  Google Scholar 

  51. Osinov A.G., Lebedev V.S. 2000. Genetic divergence and phylogeny of the Salmoninae based on allozyme data. J. Fish Biol. 57, 354–381.

    CAS  Google Scholar 

  52. Crane P.A., Seeb L.W., Seeb J.E. 1994. Genetic relationships among Salvelinus species inferred from allozyme data. Can. J. Fish Aquat Sci. 51(Suppl. 1), 182–197.

    Article  CAS  Google Scholar 

  53. Bernatchez L., Colombani F., Dodson J.J. 1991. Phylogenetic relationships among the subfamily Coregoninae as revealed by mitochondrial DNA restriction analysis. J. Fish Biol. 39(Suppl. A), 283–290.

    Article  CAS  Google Scholar 

  54. Turgeon J., Bernatchez L. 2003. Reticulate evolution and phenotypic diversity in North American ciscoes, Coregonus ssp. (Teleostei: Salmonidae): Implications for the conservation of an evolutionary legacy. Conserv. Genet. 4, 67–81.

    Article  CAS  Google Scholar 

  55. Shedko S.V., Miroshnichenko I.L., Nemkova G.A. 2012. Phylogeny of Salmonids (Salmoniformes, Salmonidae) and its molecular dating: Analysis of nuclear RAG1 gene. Russ. J. Genet. 48, 575–579.

    Article  CAS  Google Scholar 

  56. Nei M., Xu P., Glazko G. 2001. Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms. Proc. Natl. Acad. Sci. U. S. A. 98, 2497–2502.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Thorpe J.P. 1982. The molecular clock hypothesis, biochemical evolution, genetic differentiation and systematics. Annu. Rev. Ecol. Evol. Syst. 13, 139–168.

    Article  CAS  Google Scholar 

  58. Crespi B.J., Fulton M.J. 2004. Molecular systematic of Salmonidae: Combined nuclear data yields a robust phylogeny. Mol. Phylogenet. Evol. 31, 658–679.

    Article  CAS  PubMed  Google Scholar 

  59. Ferree P.M., Barbash D.A. 2009. Species-specific heterocromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 7(10), e1000234.

    Article  PubMed Central  PubMed  Google Scholar 

  60. Hughes S.E., Hawley R.S. 2009. Heterochromatin: A rapidly evolving species barrier. PLOS Biol. 7, e1000233. www.plosbiology.org.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. A. Shubina.

Additional information

Original Russian Text © E.A. Shubina, E.V. Ponomareva, A.V. Klimov, A.V. Klimova, O.S. Kedrova, 2015, published in Molekulyarnaya Biologiya, 2015, Vol. 49, No. 3, pp. 405–416.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shubina, E.A., Ponomareva, E.V., Klimov, A.V. et al. Repetitive DNA sequences as an indicator of the level of genetic isolation in fish. Mol Biol 49, 358–368 (2015). https://doi.org/10.1134/S0026893315030152

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893315030152

Keywords

Navigation