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Phylogeography of European grayling, Thymallus thymallus (Actinopterygii, Salmonidae), within the Northern Adriatic basin: evidence for native and exotic mitochondrial DNA lineages

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Abstract

Phylogeographic information on European grayling, Thymallus thymallus, is still fragmentary for the Northern Adriatic basin. In this article, we provide complete mitochondrial DNA control region sequence data of 456 grayling specimens from 21 sampling sites across distinct river drainages. Thirty-seven haplotypes were resolved and clustered into Danubian, Atlantic and Adriatic lineages. The latter clade, composed of 16 new haplotypes, was identified in 12 out of 17 Adriatic sampling sites and reached frequencies of 0.97 within single water courses of the Adige and the Po drainages. However, native Adriatic haplotypes were accompanied by Danubian and/or Atlantic variants in all cases. A positive correlation between hatchery haplotype frequency and annual stocking input pointed to a direct effect of stocking intensity on the genetic architecture of wild populations, although natural trans-basin colonisation may have additionally complicated the situation. However, both the extent and patterns of introgression between native and foreign strains, as well as microgeographic population structure within the Adriatic lineage will be clarified by future molecular surveys, based on nuclear genetic markers. Until then, conservation management must include an immediate cessation of stocking of commercial grayling stocks, as well as the prohibition of grayling translocation, even at the intra-drainage level.

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References

  • Aris-Brosou, S. & L. Excoffier, 1996. The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution 13: 494–504.

    Article  PubMed  CAS  Google Scholar 

  • Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57: 289–300.

    Google Scholar 

  • Bernatchez, L. & C. C. Wilson, 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Molecular Ecology 7: 431–452.

    Article  Google Scholar 

  • Bruford, M. W., O. Hanotte, J. F. Y. Brookfield & T. Burke, 1998. Multilocus and single locus DNA fingerprinting. In Hoelzel, A. R. (ed.), Molecular Genetic Analysis of Populations: A Practical Approach. Oxford University Press, Oxford, New York, Tokyo: 287–336.

    Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    Article  PubMed  CAS  Google Scholar 

  • Drummond, A. J. & A. Rambaut, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.

    Article  PubMed  Google Scholar 

  • Drummond, A. J., S. Y. W. Ho, M. J. Phillips & A. Rambaut, 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: e88.

    Article  PubMed  Google Scholar 

  • Duftner, N., S. Koblmüller, S. Weiss, N. Medgyesy & C. Sturmbauer, 2005. The impact of stocking on the genetic structure of European grayling (Thymallus thymallus, Salmonidae) in two alpine rivers. Hydrobiologia 542: 121–129.

    Article  CAS  Google Scholar 

  • Durand, J. D., H. Persat & Y. Bouvet, 1999. Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Molecular Ecology 8: 989–997.

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gross, R., R. Kühn, M. Baars, W. Schröder, H. Stein & O. Rottmann, 2001. Genetic differentiation of European grayling populations across the Main, Danube and Elbe drainages in Bavaria. Journal of Fish Biology 58: 264–280.

    Article  CAS  Google Scholar 

  • Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk & O. Gascuel, 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321.

    Article  PubMed  CAS  Google Scholar 

  • Gum, B., R. Gross & R. Kühn, 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 & R. Kühn, 2006. Discriminating the impact of recent human mediated stock transfer from historical gene flow on genetic structure of European grayling Thymallus thymallus L. Journal of Fish Biology 69: 115–135.

    Article  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 

  • Hewitt, G. M., 1999. Post-glacial re-colonisation of European biota. Biological Journal of the Linnean Society 68: 87–112.

    Article  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 my mitochondrial DNA analyses. Molecular Ecology 9: 1609–1624.

    Article  PubMed  CAS  Google Scholar 

  • Koskinen, M. T., I. Knizhin, C. R. Primmer, C. Schlötterer & S. Weiss, 2002. Mitochondrial and nuclear DNA phylogeography of Thymallus spp. (grayling) provides evidence of ice-age mediated environmental perturbations in the world’s oldest body of freshwater, Lake Baikal. Molecular Ecology 11: 2599–2611.

    Article  PubMed  CAS  Google Scholar 

  • Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fishes. Kottelat, Freyhof, Cornol and Berlin.

    Google Scholar 

  • Meraner, A., S. Baric, B. Pelster & J. Dalla Via, 2007. Trout (Salmo trutta) mitochondrial DNA polymorphism in the centre of the marble trout distribution area. Hydrobiologia 579: 337–349.

    Article  CAS  Google Scholar 

  • Northcote, T. G., 1995. Comparative biology and management of Arctic and European grayling (Salmonidae, Thymallus). Reviews in Fish Biology and Fisheries 5: 141–194.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ray, N., M. Currat & L. Excoffier, 2003. Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution 20: 76–86.

    Article  PubMed  CAS  Google Scholar 

  • Rice, W. R., 1989. Analysing tables of statistical tests. Evolution 43: 223–225.

    Article  Google Scholar 

  • Sabbadini, A., 2000. On Italian and Balkan grayling. In Broughton, R. (ed.), The Complete Book of Grayling. Robert Hale, London: 194–214.

    Google Scholar 

  • Salzburger, W., A. Brandstätter, A. Gilles, W. Parson, M. Hempel, C. Sturmbauer & A. Meyer, 2003. Phylogeography of the vairone (Leuciscus souffia, Risso 1826) in Central Europe. Molecular Ecology 12: 2371–2386.

    Article  PubMed  Google Scholar 

  • Seifertova, M., J. Bryja, M. Vyskocilova, N. Martinkova & A. Simkova, 2011. Multiple Pleistocene refugia and post-glacial colonization in the European chub (Squalius cephalus) revealed by combined use of nuclear and mitochondrial markers. Journal of Biogeography. doi:10.1111/j.1365-2699.2011.02661.x.

    Google Scholar 

  • Stefani, F., P. Galli, S. Zaccara & G. Crosa, 2004. Genetic variability and phylogeography of the cyprinid Telestes muticellus within the Italian peninsula as revealed by mitochondrial DNA. Journal of Zoological Systematics and Evolutionary Research 42: 323–331.

    Article  Google Scholar 

  • Storey, J. D., 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 64: 479–498.

    Article  Google Scholar 

  • Susnik, S., A. Snoj & P. Dovc, 2001. Evolutionary distinctiveness of grayling (Thymallus thymallus) inhabiting the Adriatic river system, as based on mtDNA variation. Biological Journal of the Linnean Society 74: 375–385.

    Google Scholar 

  • Susnik, S., P. Berrebi, P. Dovc, 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: 272–282.

    Article  Google Scholar 

  • Swofford, D. L., 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA.

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    PubMed  CAS  Google Scholar 

  • Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882.

    Article  PubMed  CAS  Google Scholar 

  • Tsigenopoulos, C. S., P. Kotlìk & P. Berrebi, 2002. Biogeography and pattern of gene flow among Barbus species (Teleostei: Cyprinidae) inhabiting the Italian Peninsula and neighbouring Adriatic drainages as revealed by allozyme and mitochondrial sequence data. Biological Journal of the Linnean Society 75: 83–99.

    Article  Google Scholar 

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

    Google Scholar 

  • Weiss, S., H. Persat, R. Eppe, C. Schlötterer & F. Uiblein, 2002. Complex patterns of colonisation 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 

  • Zolezzi, G., A. Bellin, M. C. Bruno, B. Maiolini & A. Siviglia, 2009. Assessing hydrological alterations at multiple temporal scales: Adige River, Italy. Water Resources Research 45: 1–15.

    Article  Google Scholar 

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Acknowledgments

This study was carried out within the framework of the project “ABaTe”, funded by the Autonomous Province of Trento under its COFUND programme. The authors thank the Fisheries Offices of the Autonomous Provinces of Bolzano/Bozen and Trento, the Province of Verona, the Environmental and Aquaculture Services Unit (IASMA-FEM), V. Adami and A. Festi as well as numerous angling associations within the Northern Adriatic basin for their great assistance during sampling activities. In addition, we would also like to thank S. Battistella (University of Trieste, Italy), B. Gum (University of TU München-Weihenstephan, Germany), C. Puzzi (GRAIA, Italy), S. Rossi (free-lance biologist, Italy), S. Salviati (Aquaprogram, Italy) and G. Unfer (BOKU, University of Vienna, Austria) for providing us with tissue samples or DNA extracts. Finally, we thank P. Gratton, C. Vernesi, S. Weiss as well as one anonymous reviewer for their constructive inputs and helpful comments and A. Daly, G. Flaim and D. B. Neale for their linguistic revision.

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Correspondence to A. Meraner.

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Handling editor: Christian Sturmbauer

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10750_2012_1109_MOESM1_ESM.pdf

Online resource 1 Sequence alignment for putative chimeric haplotypes Ad2–Ad6 with their most likely parental haplotype (PDF 104 kb)

10750_2012_1109_MOESM2_ESM.pdf

Online resource 2 Relative stocking intensity of T. thymallus within the Upper Adige region (Autonomous Province of Bolzano/Bozen) and the relationship between stocking input and hatchery haplotype frequency (PDF 73 kb)

Supplementary material 3 (DOCX 27 kb)

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Meraner, A., Gandolfi, A. Phylogeography of European grayling, Thymallus thymallus (Actinopterygii, Salmonidae), within the Northern Adriatic basin: evidence for native and exotic mitochondrial DNA lineages. Hydrobiologia 693, 205–221 (2012). https://doi.org/10.1007/s10750-012-1109-x

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