Genetic variation of European grayling (Thymallus thymallus) populations in the Western Balkans
In order to elucidate genetic composition of European grayling (Thymallus thymallus) populations in the Western Balkans, the partial mitochondrial DNA (mtDNA) control region was sequenced and 12 microsatellite loci genotyped in 14 populations originating from tributaries of the Adriatic and Danube drainages. Eleven mtDNA haplotypes were found, one confined to the Adriatic clade, one to the Alpine group and the rest to the ‘Balkan’ grayling phylogenetic clade. Haplotypes from the Balkan clade were confined to the Danube drainage and constituted two groups: northern group with haplotypes found in the Slovenian part of the Danube drainage, and southern group, consisting from Bosnia–Herzegovina and Montenegro. Substantial genetic distance between northern and southern groups of haplotypes (0.75–1.8%) and well supported divisions within the northern group indicate very structured grayling population within the studied Danube basin that most probably did not evolve due to vicariance but rather as a consequence of multiple colonization waves that might have occurred during the Pleistocene. Furthermore, genetic distance of ~4% between Adriatic and Danube populations’ haplotypes, suggest that their separation occurred in mid-Pliocene. These findings imply a complex colonization pattern of the Western Balkans drainages. Microsatellite data also confirm high genetic diversity in Western Balkans populations of grayling (on average 7.5 alleles per microsatellite locus and H exp 0.58). Limited stocking activities were detected based on microsatellites and mtDNA data. Regarding current knowledge of grayling phylogeography appropriate management strategies were proposed to preserve unique, autochthonous grayling populations in Western Balkan.
KeywordsEuropean grayling Western Balkans Genetic diversity mtDNA Microsatellites Evolutionary significant units
This study was supported by the Slovenian Research Agency (ARRS) Research programme P4-0220, the Ministry of Science and Technological Development of the Republic of Serbia (Grant No. 173045), the Federal Ministry of Education and Science of Bosnia and Herzegovina (Grant No. 11-14-21727.1/07), and the Agency for Management of Sava River Basin (Grant No. 10-1/52-1/08). Many thanks go to Nenad Lazarević for graphic support.
- Baars, M., E. Mathes, H. Stein & U. Steinhörster, 2001. Die Äsche. Die Neue Brehm-Bücherei, Westarp Wissenschaften, Hohenwarsleben: 640 pp. (in German).Google Scholar
- Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996–2004. GENETIX v. 4.04, Logiciel sous WindowsTM pour la Génétique des Populations. Université Montpellier 2, Laboratoire Génome et Population, Montpellier.Google Scholar
- Froufe, E., I. Knizhin & S. Weiss, 2005. Phylogenetic analysis of the genus Thymallus (grayling) based on mtDNA control region and ATPase 6 genes, with inferences on control region constraints and broad-scale Eurasian phylogeography. Molecular Phylogenetics and Evolution 34: 106–117.PubMedCrossRefGoogle Scholar
- Gardiner, R., 2000. The origins and present distribution of grayling. In Broughton, R. (ed.), The Complete Book on Grayling. Robert Hale Publishers, London: 15–22.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: 441–452. ISBN 0521781426.Google Scholar
- Goudet, J., 2002. FSTAT, a program to estimate and test gene diversities and fixation indices (version 184.108.40.206). http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 15 October 2009.
- Gum, B., 2007. Genetic Characterisation of European Grayling (Thymallus thymallus) Populations: Implications for Conservation and Management. Dissertation, Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt, TU München: 167 pp.Google Scholar
- Janković, D. 1960. Sistematika i ekologija lipljena (Thymallus thymallus L.) u Jugoslaviji, Vol. 7. Biološki Institut, Beograd: 145 pp.Google Scholar
- Jesenšek, D. & S. Šumer, 2004. Adriatic grayling (Thymallus thymallus, Linnaeus, 1758) in the Soča River basin, Slovenia: action plan. Ribiška družina/Ente Tutela Pesca del Friuli Venezia Giulia, Tolmin/Udine: 32 pp.Google Scholar
- Kalamujić, B., 2008. Molecular-Genetic Diversity of Grayling (Thymallus thymallus L.) Populations in Bosnia and Herzegovina. Master thesis in Bosnian, English summary, Faculty of Science, University of Sarajevo.Google Scholar
- Kalamujić, B., N. Pojskić, A. Durmić-Pasić, R. Škrijelj & R. Hadžiselimović, 2007. Genetic diversity of grayling (Thymallus thymallus L.) populations in Bosnia–Herzegovina, Book of abstracts of XII European Congress of Ichthyology, Cavtat, Croatia: 32 pp.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.PubMedCrossRefGoogle Scholar
- Koskinen, M. T., I. Knizhin, C. R. Primmer, C. Schlötterer & S. Weiss, 2002c. 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.PubMedCrossRefGoogle Scholar
- Langella, O., 2002. Populations 1.2.28. Logiciel de génétique des populations. Laboratoire Populations, génétique et évolution, CNRS UPR 9034, Gif-sur-Yvette. http://www.cnrs-gif.fr/pge/. Accessed 10 October 2009.
- Ovidio, M., D. Parkinson, D. Sonny & J. C. Philippart, 2004. Spawning movements of the European grayling Thymallus thymallus in River Aisne. Folia Zoologica 53: 87–98.Google Scholar
- Penck, A. & E. Brückner, 1909. Die Alpen im Eiszeitalter. Taunitz, Leipzig: 1199 pp.Google Scholar
- Sušnik, S., A. Snoj & P. Dovč, 2001. Evolutionary distinctness of grayling (Thymallus thymallus) inhabiting the Adriatic river system, as based on mtDNA variation. Biological Journal of Linnean Society 74: 375–385.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.PubMedCrossRefGoogle Scholar
- Swofford, D. L., 2000. PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods). b-VERSION 4.0. Sinauer Associates, Sunderland, MA.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: 223–247.Google Scholar
- Waples, R. S., 1991. Pacific Salmon, Oncorhynchus spp. and the definition of species under the endangered species act. Marine Fisheries Review 53: 11–22.Google Scholar