Abstract
The Eurasian beaver (Castor fiber) represents an uncommon example of an endangered species in which the restoration programs proved a spectacular success and led to enormous spatial and demographic expansion. Documented reintroduction of beavers in Poland has been conducted using animals of the eastern European origin, most likely derived from the eastern mtDNA lineage. However demographic and spatial expansion of beavers from Germany, which represent the western lineage, may have led to admixture of these two genetically distinct entities in Poland. We detected significant genetic differentiation between the populations from W and NE Poland both in mitochondrial DNA control region and microsatellites, but also substantial admixture including apparent first-generation migrants between regions. Our results indicate that beavers from the western mtDNA lineage have contributed considerably to the Polish population, particularly in W Poland. As there have been no adequately documented translocations of beavers from the western European populations to Poland, the observed situation appears to result from natural migration or range expansion from the west. In contrast to previous findings we detected a substantial diversity in mtDNA control region, which indicates that either the variation in relict populations has been underestimated, or that additional relict beaver populations survived at the end of the 19th century in Poland and Germany as indicated by considerable similarity of ancient and extant mtDNA haplotypes. The implications of our findings for beaver conservation and management are discussed.
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Abbot, R., Albach, D., Ansell, S., etal., 2013. Hybridization and speciation. J. Evol. Biol. 26, 229–246.
Avise, J.C., 2004. Phylogeography. The History and Formation of Species. Harvard University Press, Cambridge, MA.
Babik, W., Durka, W., Radwan, J., 2005. Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol. Ecol. 14, 4249–4257.
Barták, A., Vorel, S., Simová, P., Pus, V., 2013. Spatial spread of Eurasian beavers in river networks: a comparison of range expansion rates. J. Anim. Ecol. 82, 587–597.
Cheney, L.C., 1995. An Assessment of Genetic Variation Within and Between Sea Otter (Enhydra lutris) Populations of Alaska and California. Moss Landing Marine Laboratories, California State University, San Jose.
Crawford, J., Liu, Z., Nelson, T., Nielsen, C, Bloomquist, C, 2008. Isolation and characterization of microsatellite loci in the beaver (Castor canadensis). Mol. Ecol. Resour. 8, 616–618.
Crawford, J.C., Liu, Z., Nelson, T.A., Nielsen, C.K., Bloomquist, C.K., 2009. Genetic population structure within and between beaver (Castor canadensis) populations in Illinois. J. Mammal. 90, 373–379.
Currat, M., Ruedi, M., Petit, R.J., Excoffier, L., 2008. The hidden side of invasions: massive introgression by local genes. Evolution 62, 1908–1920.
Czech, A., 2010. Bóbr - budowniczy i inzynier. Fundacja Wspierania Inicjatyw Ekologicznych, Kraków.
Dawson, K.J., Belkhir, K., 2001. A Bayesian approach to the identification of panmictic populations and the assignment of individuals. Genet. Res. 78, 59–77.
Djoshkin, W.W., Safonow, W.G., 1972. Die BiberderAltenund Neuen Welt. Wittenberg, A. Ziemsen Verlag.
Ducroz, J.F., Stubbe, M., Saveljev, A., Heidecke, D., Samjaa, R., Ulevicius, A., Stubbe, A., Durka, W., 2005. Genetic variation and population structure of the Eurasian beaver Castor fiber in Eastern Europe and Asia based on mtDNA sequences. J. Mammal. 86, 1059–1067.
Durka, W., Babik, W., Ducroz, J-F., Heidecke, D., Rosell, F., Samjaa, R., Saveljev, A.P., Stubbe, A., Ulevicius, A., Stubbe, M., 2005. Mitochondrial phylogeography of the Eurasian beaver Castor fiber L. Mol. Ecol. 14, 3843–3856.
Dzie, ciołowski, R., Gozdziewski, J., 1999. The reintroduction of the European beaver Castor fiber in Poland: a success story. In: Busher, P., Dzie, ciołowski, R. (Eds.), Beaver Protection, Management and Utilization in Europe and North America. Kluwer Academic/Plenum Publishers, New York, pp. 31–35.
Earl, D.A.,vonHoldt, B.M., 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Res. 4, 359–361.
Ellegren, H., Hartman, G., Johansson, M., Andersson, L., 1993. Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc. Natl. Acad. Sci. U.S.A. 98, 8150–8153.
Evanno, G., Regnaut, U.T., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.
Excoffier, L, Foll, M., Petit, R.J., 2009. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501.
Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
Frahnert, S., 2000. Ontogenetic changes of cranial proportions in eaver, Castor fiber L., 1758 (Rodentia Castoridae): taxonomical mplicationsand functional aspects. Bonner Zoologische Beiträge 49, 131–153 [in German].
Frankham, R., Ballou, J.D., Briscoe, DA, 2002. Conservation Genetics. Cambridge University Press, Cambridge.
Frosch, C, Haase, P., Nowak, C, 2012. First set of microsatellite markers for genetic characterization of the Eurasian beaver (Castor fiber) based on tissue and hair samples. Eur. J. Wildl. Res. 57, 679–682.
Goudet, J., 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Hered. 86, 485–486.
Guo, S., Thompson, E.A., 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361–372.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.
Halley, D.J., 2011. Sourcing Eurasian beaver Castor fiber stock for reintroductions in Great Britain and Western Europe. Mammal Rev. 41, 40–53.
Halley, D.J., Rosell, F., 2002. The beaver’s reconquest of Eurasia: status, population development and management of a conservation success. Mammal Rev. 32, 153–178.
Hellborg, L. Ellegren, H., 2003.Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific fragments. Mol. Ecol. 12, 283–291.
Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. B 359, 183–195.
Hofreiter, M., Serre, D., Rohland, N., Rabeder, G., Nagel, D., Conard, N., Münzel, S., Pääbo, S., 2004. Lack of phylogeography in European mammals before the last glaciation. Proc. Natl. Acad. Sci. U.S.A. 101, 12963–12968.
Hofreiter, M., Stewart, J., 2009. Ecological change, range fluctuations and population dynamics during the pleistocene. Curr. Biol. 19, R584–R594.
Horn, S., Teubner, J., Heidecke, D., 2010. Mitochondrial DNA of beavers (Castor) in Germany. Artenschutzreport 26, 72–78.
Horn, S., Durka, W., Wolf, R., Ermala, A., Stubbe, A., Stubbe, M., Hofreiter, M., 2011. Mitochondrial genomes reveal slow rates of molecular evolution and the timing of speciation in beavers (Castor), one of the largest rodent species. PLoS ONE 6.
Horn, S., Prost, S., Stiller, M., Makowiecki, D., Kuznetsova, T., Benecke, N., Pucher, E., Hufthammer, A.K., Schouwenburg, C, Shapiro, B., Hofreiter, M., 2014. Ancient mitochondrial DNA and the genetic history of Eurasian beaver (Castor fiber) in Europe. Mol. Ecol. 23, 1717–1729.
Jakobsson, M., Rosenberg, N., 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23,1801-1806.
Kautenburger, R., Sander, A., 2008. Population genetic structure in natural and reintroduced beaver (Castor fiber) populations in Central Europe. Anim. Biodivers. Conserv. 31, 25–35.
Keller, S.R., Taylor, D.R., 2010. Genomic admixture increases fitness during a biological invasion. J. Evol. Biol. 23, 1720–1731.
Kolbe, J.J., Larson, A., Losos, J.B., De Queiroz, K., 2008. Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biol. Lett. 4, 434–437.
Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
McDevitt, A.D., Zub, K., Kawałko, A., Oliver, M.K., Herman, J.S., Wójcik, J.M., 2012. Climate and refugial origin influence the mitochondrial lineage distribution of weasels (Mustela nivalis) in a phylogeographic suture zone. Biol. J. Linn. Soc. 106, 57–69.
Moritz, C, 1994. Defining ‘evolutionary significant units’ for conservation. Trends Ecol. Evol. 9, 373–375.
Nolet, B.A., Rossel, F., 1998. Comeback of the beaver Castor fiber: an overview of old and new conservation problems. Biol. Conserv. 83, 165–173.
Pelz-Serrano, K., Munguia-Vega, A., Piaggio, A.J., Neubaum, M., Munclinger, P., Pártl, A., van Riber, C, Culver, M., 2009. Development of nine new microsatellite loci for the American beaver, Castor canadensis (Rodentia: Castoridae), and crossspecies amplification in the European beaver, Castor fiber. Mol. Ecol. Resour. 9, 551–554.
Petit, R.J., Excoffier, L, 2009. Gene flow and species delimitation. Trends Ecol. Evol. 24, 386–393.
Piry, S., Luikart, G., Cornuet, J-M., 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 95, 536–539.
Pritchard, J.K., Stevens, M., Donnely, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Rannala, B., Mountain, J.L., 1997. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA 94, 9197–9201.
Rosell, F., Campbell-Palmer, R.I., Parker, H., 2012. More genetic data are needed before populations are mixed: response to Sourcing Eurasian Beaver Castor fiber stock for reintroductions in Great Britain and Western Europe. Mammal Rev. 42, 319–324.
Rousset, F., 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106.
Saccone, C, Attimonelli, M., Sbisa, E., 1987. Structural elements highly preserved during the evolution of the D-loop-containing region in vertebrate mitochondrial-DNA. J. Mol. Evol. 26, 205–211.
Schwab, G., Lutschinger, G., 2001. The return of the beaver (Castor fiber) to the Danube watershed. In: Czech, A., Schwab, G. (Eds.), The European Beaver in a New Millennium. Carpathian Heritage Society, Cracow, Poland, pp. 47–50.
Senn, H., Ogden, R., Frosch, C, Syruckova, A., Campbell-Palmer, R., Munclinger, P., Durka, W., Kraus, R., Saveljev, A., Nowak, C, Stubbe, A., Stubbe, M., Michaux, J., Lavrov, V., Samiya, R., Ulevicius, A., Rosell, F., 2014. Nuclear and mitochondrial genetic structure in the Eurasian beaver (Castor fiber) - implications for future reintroductions. Evolutionary Applications. (in press).
Senn, H., Ogden, R., Cezard, T., Gharbi, K., Iqbal, Z., Johnson, E., Kamps-Hughes, N., Rosell, F., McErwing, R., 2013. Reference-free SNP discovery for the Eurasian beaver from restriction site-associated DNA paired-end data. Mol. Ecol. 22, 3141–3150.
Shafer, A.B.A., Cullingham, C.I., Côté, S.D., Coltman, D.W., 2010. Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Mol. Ecol. 19, 4589–4621.
Swofford, D.L., 2003. PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sinauer Associates, Sunderland, MA.
Taberlet, P., Fumagalli, L, Wust-Saucy, A.G., Cosson, J.F., 1998. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464.
Vähä, J.P., Primmer, C.R., 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 15, 63–72.
Żurowski, W., 1979. Preliminary results of European beaver reintroduction in the tributary streams of the Vistula River. Acta Theriol. 24, 85–91.
Żurowski, W., 1980. Bóbreuropejski w Polsce. Przeglad Hodowlany 11, 18–23.
Żurowski, W., 1992. Castor fiber (Linne, 1758) - Bóbreuropejski. In: Głowacinski, Z. (Ed.), Polska czerwona ksie˛ga zwierzat. PWRiL, Warszawa, pp. 56–59.
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Biedrzycka, A., Konior, M., Babik, W. et al. Admixture of two phylogeographic lineages of the Eurasian beaver in Poland. Mamm Biol 79, 287–296 (2014). https://doi.org/10.1016/j.mambio.2014.04.005
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DOI: https://doi.org/10.1016/j.mambio.2014.04.005