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Phylogenetic and population genetic analysis of Thymallus thymallus (Actinopterygii, Salmonidae) from the middle Volga and upper Ural drainages

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Abstract

The evolutionary relationship of grayling populations from the Kama and upper Ural drainage was studied, and the genetic diversity of the local populations was assessed. The complete mitochondrial DNA control region was sequenced and 12 microsatellite loci genotyped. Five previously undescribed closely related haplotypes (Caspian clade) were detected. The Caspian and previously reported Scandinavian clade formed a Caspio–Scandinavian group that was found to be the closest relative to the Balkan clade of European grayling. Based upon the molecular results, paleogeological information and a molecular clock of 0.5% change per million years, it appears the Caspio–Scandinavian group split some 0.6 million years ago (95% HPD = 0.33–0.92 mya), while the Balkan clade separated about 1 mya, in the Pleistocene. The sister relationship between Caspian and Scandinavian haplotypes implies that, at some time over that period, the Caspian basin might have been a corridor for dispersal connecting eastern and northern Europe. Microsatellite analysis revealed relatively large inter-population genetic differentiation among the Caspian sample set, pointing to genetically distinct populations that are deserving of special attention in terms of management and conservation.

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References

  • Abdrachmanov, R. F., V. I. Martin, V. G. Popov, A. P. Rozhdestvenski, A. I. Smirnov & A. I. Travkin, 2002. Karst of Bashkortostan. Informreklama, Ufa. (in Russian).

  • Aladin, N. B. & I. S. Plotnikov, 2000. Danger of large-scale ecological catastrophe in the Caspian (The comparative analysis of causes and effects of ecological crises in the Aral and Caspian). The Caspian Bulletin 4: 112–126. (in Russian).

    Google Scholar 

  • Askeyev, O. V., I. V. Askeyev, S. P. Monahov, S. Marić, A. Snoj, N. M. Yanyabaev, A. O. Askeyev & D. N. Galimova, 2013. Historical and current distribution of the four species and forms of Salmoniformes in the territory of the Volga and Ural basin. In Askeyev, V. I., V. O. Askeyev, V. Dmitry & V. Ivanov (eds), Proceedings of the Third Russian Scientific Conference on the Dynamics of Modern Ecosystems in the Holocene. Otechestvo, Kazan: 15–23. (in Russian).

  • Askeyev, A., S. Monakhov, I. Askeyev & O. Askeyev, 2014. Rare and endangered fish species distribution in relation to environmental gradients, Tatartstan republic, Russia. In Ivanov, V. (ed.), Proceeding of Scientific Works of Institute of Problems Ecology and Mineral Wealth. Tatarstan Academy of Sciences, Otechestvo, Kazan: 3–15. (in Russian).

    Google Scholar 

  • Berg, L. S., 1948. Freshwater fishes of the USSR and adjacent countries. Part 1, 4th ed. USSR Academy of Sciences, Moscow & Leningrad. (in Russian).

    Google Scholar 

  • Chibilev, A. A., 1993. Rare species of fishes of the Orenburg region and their conservation. Nauka, Ekaterinburg. (in Russian).

    Google Scholar 

  • Clement, M., D. Posada & K. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.

    Article  PubMed  CAS  Google Scholar 

  • Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29(8): 1969–1973.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  PubMed  CAS  Google Scholar 

  • Froufe, E., I. Knizhin, M. T. Koskinen, C. R. Primmer & S. Weiss, 2003. Identification of reproductively isolated lineages of Amur grayling (Thymallus grubii Dybowski 1869): concordance between phenotypic and genetic variation. Molecular Ecology 12: 2345–2355.

    Article  PubMed  CAS  Google Scholar 

  • Gibbard, P. & T. van Kolfschoten, 2004. The pleistocene and holocene epochs. In Gradstein, F. M., J. G. Ogg & A. G. Smith (eds), A Geologic Time Scale. Cambridge University Press, Cambridge. ISBN ISBN 0521781426: 441–452.

  • Gorecky, G. I., 1966. Formation of Volga River Valley in the Early and Middle Quaternary. Nauka Press, Moscow. (in Russian).

    Google Scholar 

  • Gum, B., R. Gross & R. Kuehn, 2005. Mitochondrial and nuclear DNA phylogeography of European grayling (Thymallus thymallus): evidence for secondary contact zones in central Europe. Molecular Ecology 14: 1707–1725.

    Article  PubMed  CAS  Google Scholar 

  • Gum, B., R. Gross & J. Geist, 2009. Conservation genetics and management implications for European grayling, Thymallus thymallus: synthesis of phylogeography and population genetics. Fisheries Management and Ecology 16: 37–51.

    Article  Google Scholar 

  • Hasegawa, M., H. Kishino & T. Jano, 1985. Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.

    Article  PubMed  CAS  Google Scholar 

  • Koskinen, M. T., E. Ranta, J. Piironen, A. Veselov, S. Titov, T. O. Haugen, J. Nilsson, M. Carlstein & C. R. Primmer, 2000. Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Molecular Ecology 9: 1609–1624.

    Article  PubMed  CAS  Google Scholar 

  • Kvasov, D. D., 1975. Late Quaternary History of Large Lakes and Inland Seas of Eastern Europe. Nauka Press, Lenningrad. (in Russian).

    Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    Article  PubMed  CAS  Google Scholar 

  • Marić, S., A. Razpet, V. Nikolić & P. Simonović, 2011. Genetic differentiation of European grayling (Thymallus thymallus) populations in Serbia, based on mitochondrial and nuclear DNA analyses. Genetics Selection Evolution 43: 2.

    Article  Google Scholar 

  • Marić, S., B. Kalamujić, A. Snoj, A. Razpet, L. Lukić-Bilela, N. Pojskić & S. Sušnik Bajec, 2012. Genetic variation of European grayling (Thymallus thymallus) populations in the Western Balkans. Hydrobiologia 691: 225–237.

    Article  Google Scholar 

  • Meraner, A. & A. Gandolfi, 2012. Phylogeography of European grayling, Thymallus thymallus (Actinopterygii, Salmonidae), within the Northern Adriatic basin: evidence for native and exotic mitochondrial DNA lineages. Hydrobiologia 693(1): 205–221.

    Article  CAS  Google Scholar 

  • Obedientova, G. V., 1975. Formation of river systems of Russian Plain. Nedra, Moscow. (in Russian).

    Google Scholar 

  • Ozhiganov, D. G., 1964. Bashkir ASSR and Orenburg Region. Part 1. In Ozhiganov, D. G. (ed.), Geology of the USSR. Nedra, Moscow: 656 pp. [The geological description, vol XIII]. (in Russian).

  • Penck, A. & E. Brückner, 1909. Die Alpen im Eiszeitalter. Taunitz, Leipzig: 1199 pp.

    Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Shaposhnikova, G. H., 1964. Biology and Distribution of Fish in Ural Type of Rivers. Nauka Press, Moscow. (in Russian).

    Google Scholar 

  • Stadler, T., 2009. On incomplete sampling under birth-death models and connections to the sampling-based coalescent. Journal of Theoretical Biology 261(1): 58–66.

    Article  PubMed  Google Scholar 

  • Starobogatov, Y. I., 1970. Fauna of Molluscs and Zoogeographical Division of Continental Waters of the World. Academy of Sciences of USSR, Institute of Zoology, Leningrad. (in Russian).

    Google Scholar 

  • Sušnik, S., P. Berrebi, P. Dovč, M. M. Hansen & A. Snoj, 2004. Genetic introgression between wild and stocked salmonids and the prospects for using molecular markers in population rehabilitation: the case of the Adriatic grayling (Thymallus thymallus L. 1785). Heredity 93: 273–282.

    Article  PubMed  Google Scholar 

  • Svetovidov, A. N., 1936. Graylings (genus Thymallus, Cuvier) of Europe and Asia. Proceedings of Institute of Zoology Academy of Sciences USSR 3: 183–301. (in Russian).

    Google Scholar 

  • Swatdipong, A., A. Vasemägi, M. T. Koskinen, P. Piironen & C. R. Primmer, 2009. Unanticipated population structure of European grayling in its northern distribution: implications for conservation prioritization. Frontiers in Zoology 6: 6.

    Article  PubMed  PubMed Central  Google Scholar 

  • The Red Book of the Orenburg region, 1998. (Animals and Plants.). Orenburg Publishing House, Orenburg. (in Russian).

  • The Red Book of the Republic of Bashkortostan, 2004. Part 3. (Animals.). Kitap, Ufa. (in Russian).

  • The Red Book of the Republic of Tatarstan, 2006. (Animals, Plants, Fungi.) 2nd edn. Idel-Press, Kazan. (in Russian).

  • The Red Data Book of Russian Federation, 2001. (Animals.). AST-Astrel Publishers, Moscow. (in Russian).

  • 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: 223–247.

    Google Scholar 

  • Van Oosterhout, C., W. F. D. Hutchinson, P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  Google Scholar 

  • Weiss, S., H. Persat, R. Eppe, C. Schlötterer & F. Uiblein, 2002. Complex patterns of colonization and refugia revealed for European grayling Thymallus thymallus, based on complete sequencing of the mitochondrial DNA control region. Molecular Ecology 11: 1393–1407.

    Article  PubMed  CAS  Google Scholar 

  • Yakhimovich, V. L., V. K. Nemkova, A. V. Sydnev, F. I. Suleimanova, G. A. Khabibullina, T. I. Sherbakova & A. G. Yakovlev, 1987. The Pleistocene of the Fore-Urals. Nauka Press, Moscow. (in Russian).

    Google Scholar 

  • Zinoviev, E., 1969. Characteristics of feeding of grayling in different water types in Kama River basin. In Biology of Fish in Middle Kama basin, Vol. 195. Proceedings of Perm State University: 83–93. (in Russian).

  • Zinoviev, E., 2008. Ecological standards of river and streams morphotypes of grayling Thymallus thymallus (Linnaeus, 1758) in Kama basin. In Biology and Ecology of Fishes in Kama Region. Between Universities Proceeding of Scientific Work, Vol. 2. Perm: 32–40. (in Russian).

  • Zinoviev, E., 2005. Ecotypes of grayling fish (Thymallidae, Salmoniformes). Russian Journal of Ecology 5: 385–389. (in Russian).

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Slovenian Research Agency, and the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 173045). The authors wish to express their gratitude to the administration of Bashkirian and Shulgan-Tash nature reserves and to the Director of the Institute for Problems of Ecology and Mineral Wealth, Mr. Shagidullin R.R., for their irrepressible support during the field surveys. Many thanks go to I. F. Wilson for English revision of the manuscript.

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Authors and Affiliations

  1. Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski Trg 16, 11001, Belgrade, Serbia

    Saša Marić

  2. Institute for Problems of Ecology and Mineral Wealth, Tatarstan Academy of Sciences, Daurskaya 28, 420087, Kazan, Tatarstan Republic, Russian Federation

    Igor V. Askeyev, Oleg V. Askeyev & Sergey P. Monakhov

  3. Department of Animal Science, Biotechnical Faculty, University of Ljubljana, Groblje 3, 1230, Domžale, Slovenia

    Jernej Bravničar & Aleš Snoj

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  1. Saša Marić
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  2. Igor V. Askeyev
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  3. Oleg V. Askeyev
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  4. Sergey P. Monakhov
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Correspondence to Saša Marić.

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Handling editor: Christian Sturmbauer

Electronic supplementary material

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10750_2014_1951_MOESM1_ESM.jpg

A detailed map of the grayling extension along the whole river network shown in Fig. 1 (solid blue lines for known extension, dotted red line for presumed extension). Codes of sample site locations are reported in Table 1. (JPEG 3766 kb)

10750_2014_1951_MOESM2_ESM.doc

Estimated K values (number of genetic clusters) from STRUCTURE runs using the ΔK method. L(K), posterior probability of K; stdev, standard deviation of L(K) from seven independent runs; ΔK, an ad hoc quantity, predictor of the real number of clusters (Evanno et al., 2004), best ΔK is colored. (DOC 32 kb)

10750_2014_1951_MOESM3_ESM.doc

A synthesis of geographical plio-pleistocene history literature in Russian (references in bold are in Cyrillic). (DOC 33 kb)

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Marić, S., Askeyev, I.V., Askeyev, O.V. et al. Phylogenetic and population genetic analysis of Thymallus thymallus (Actinopterygii, Salmonidae) from the middle Volga and upper Ural drainages. Hydrobiologia 740, 167–176 (2014). https://doi.org/10.1007/s10750-014-1951-0

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