Genetic analysis of Eurasian otters (Lutra lutra) reveals high admixture in Finland and pronounced differentiation in Sweden
Abstract
A number of mammal species in Europe, including the Eurasian otter (Lutra lutra), have experienced a decline in population size in the 20th century due to persecution, environmental pollution and ongoing habitat fragmentation. This has often led to a substantial loss of genetic diversity which may threaten population viability. While otters have been studied in some detail genetically, the northern part of the Fennoscandian range has not been covered well so far. By explicitly focussing on the genetics of otter populations from northern Sweden and Finland we aimed at closing that gap. To infer their genetic structure and diversity, we analysed sequences of the mitochondrial control region and 12 nuclear microsatellite markers in 197 Eurasian otters from Sweden and Finland. Variability of the mitochondrial control region was low overall but still revealed previously undetected haplotypes unique to the Finnish otter population. Expected heterozygosities in Fennoscandia were within the range previously reported.
Bayesian cluster analysis of our microsatellite data revealed genetic structuring of the Swedish otter populations. In contrast, we observed a high degree of admixture among the Finnish populations that we also found at the geographic border of the two countries (Lapland).
Admixed ancestry in Finnish otters suggests that gene flow from the Swedish to Central European populations is potentially facilitated via the Finnish otter populations connecting the Swedish animals with otter populations in mainland Europe.
Keywords
Fennoscandia Isolation by distance Lutra lutra Microsatellites Mitochondrial DNAPreview
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References
- Allendorf, F.W., Luikart, G., 2007. Conservation and the Genetics of Populations. Blackwell Publishing, Malden, Oxford, Carlton.Google Scholar
- Arrendal, J., Walker, C.W., Sundqvist, A.K., Hellborg, L., Vilà, C., 2004. Genetic evaluation of an otter translocation program. Conserv. Genet. 5, 79–88.CrossRefGoogle Scholar
- Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.CrossRefGoogle Scholar
- Cassens, I., Tiedemann, R., Suchentrunk, F., Hartl, G.B., 2000. Mitochondrial DNA variation in the European Otter (Lutra lutra) and the use of spatial autocorrelation in conservation. J. Hered. 91, 31–35.Google Scholar
- Cederberg, H., Sandström, C., Rannug, U., Helander, B., 2003. Genetic variation based on DNA fingerprinting in two white-tailed sea eagle populations in Sweden. In: Helander, B, Marquiss, M, Bowerman, W (Eds.), Sea Eagle 2000. Swedish Society for Nature Conservation/SNF and Åtta 45 Tryckeri AB, Stockholm.Google Scholar
- Dallas, J.F., Piertney, S.B., 1998. Microsatellite primers for the European otter. Mol. Ecol. 7, 1248–1251.Google Scholar
- Elmeros, M., Hammershøj, M., Madsen, A.B., Søgaard, B., 2006. Recovery of the otter Lutra lutra in Denmark monitored by field survey and collection of carcasses. Hystrix 17 (1), 17–28.Google Scholar
- Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.CrossRefGoogle Scholar
- Excoffier, L., Laval, G., Schneider, S., 2005. ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinf. Online 1, 47–50.Google Scholar
- 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.PubMedPubMedCentralGoogle Scholar
- Ferrando, A., Lecis, R., Domingo-Roura, X., Ponsà, M., 2008. Genetic diversity and individual identification of reintroduced otters (Lutra lutra) in North-eastern Spain by DNAgenotyping of spraints. Conserv. Genet. 9 (1), 129–139.CrossRefGoogle Scholar
- Finnegan, L.A., Néill, L.Ó., 2010. Mitochondrial DNA diversity of the Irish otter Lutra lutra, population. Conserv. Genet. 11, 1573–1577.CrossRefGoogle Scholar
- Frankham, R., Ballou, J.D., Briscoe, D.A., 2004. A Primer of Conservation Genetics. Cambridge University Press, Cambridge, NY etc.CrossRefGoogle Scholar
- Goudet, J., 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Hered. 86, 485–486.CrossRefGoogle Scholar
- Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/97/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
- Honnen, A.-C., Petersen, B., Kassens, L., Elmeros, M., Roos, A., Sommer, R., Zachos, F.E., 2011. Genetic structure of Eurasian otter Lutra lutra, Carnivora: Mustel-idae populations from the western Baltic Sea region and its implications for the recolonisation of north-western Germany. J. Zool. Syst. Evol. Res. 49, 169–175.CrossRefGoogle Scholar
- Hubisz, M.J., Falush, D., Stephens, M., Pritchard, J.K., 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. 9, 1322–1332.CrossRefGoogle Scholar
- Jensen, J.L., Bohonak, A.J., Kelley, S.T., 2005. Isolation by distance web service. BMC Genet. 6, 13.PubMedPubMedCentralCrossRefGoogle Scholar
- Johnson, W.E., Onorato, D.P., Roelke, M.E., Land, E.D., Cunningham, M., Belden, R.C., McBride, R., Jansen, D., Lotz, M., Shindle, D., Howard, J., Wildt, D.E., Penfold, L.M., Hostetler, J.A., Oli, M.K., O’Brien, S.J., 2010. Genetic restoration of the Florida panther. Science 329, 1641–1645.PubMedCrossRefPubMedCentralGoogle Scholar
- Kalz, B., Jewgenow, K., Fickel, J., 2006. Structure of anotter (Lutralutra) population in Germany—results of DNA and hormone analyses from faecal samples. Mamm. Biol. 71, 321–335.CrossRefGoogle Scholar
- Kocher, T.D., Thomas, W.K., Meyer, A., Edward, S.V., Pääbo, S., Villablanca, F.X., Wilson, A.C, 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Nat1. Acad. Sci. U.S.A. 86, 6196–6200.CrossRefGoogle Scholar
- Koelewijn, H.P., Pérez-Haro, M., Jansman, H. a. H, Boerwinkel, M.C., Bovenschen, J., Lammertsma, D.R., Niewold, F.J.J., Kuiters, A.T., 2010. The reintroduction of the Eurasian otter Lutra lutra into the Netherlands: hidden life revealed by noninvasive genetic monitoring. Conserv. Genet. 11 (2), 601–614.CrossRefGoogle Scholar
- Kruuk, H., 2006. Otters. Ecology, Behaviour and Conservation. Oxford University Press, Oxford.CrossRefGoogle Scholar
- Lanszki, J., Hidas, A., Szentes, K., Révay, T., Lehoczky, I., Jeney, Z., Weiss, S., 2010. Genetic structure of otter (Lutra lutra) populations from two fishpond systems in Hungary. Mamm. Biol. 75, 447–450.CrossRefGoogle Scholar
- Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.PubMedPubMedCentralCrossRefGoogle Scholar
- Maran, T., Skumatov, D., Palazón, S., Gomez, A., Põdra, M., Saveljev, A., Kranz, A., Libois, R., Aulagnier, S., 2011. Mustela lutreola. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2, (https://doi.org/www.iucnredlist.org).
- Mucci, N., Pertoldi, C., Madsen, A.B., Loeschke, V., Randi, E., 2004. Extremely low mitochondrial DNA control-region sequence variation in the otter Lutra lutra population of Denmark. Hereditas 130, 331–336.CrossRefGoogle Scholar
- Mucci, N., Arrendal, J., Ansorge, H., Bailey, M., Bodner, M., Delibes, M., Ferrando, A., Fournier, P., Fournier, C., Godoy, J.A., Hajkova, P., Hauer, S., Heggberget, T.M., Heidecke, D., Kirjavainen, H., Krueger, H.H., Kvaloy, K., Lafontaine, L., Lanszki, J., Lemarchand, C., Liukko, U.M., Loeschke, V., Ludwig, G., Madsen, A.B., Mercier, L., Ozolins, J., Paunovic, M., Pertoldi, C., Piriz, A., Progioni, C., Santos-Reis, M., Sales Luis, T., Stjernberg, T., Schmid, H., Suchentrunk, F., Teubner, J., Tornberg, R., Zinke, O., Randi, E., 2010. Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe. Conserv. Genet. 11, 583–599.CrossRefGoogle Scholar
- Olsson, M., Sandegren, F., 1991. Otter survival and toxic chemicals—implication for otter conservation programmes. In: Proceedings V. International Otter Colloquium, Hankensbüttel 1989. In: Reuther, C., Röchert, R (Eds.), Habitat 6, pp. 191–200.Google Scholar
- Paetkau, D., Calvert, W., Stirling, I., Strobeck, C., 1995. Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4, 347–354.CrossRefGoogle Scholar
- Paetkau, D., Slade, R., Burden, M., Estoup, A., 2004. Genetic assignment method fort he direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol. Ecol. 13 (1), 55–65.PubMedCrossRefGoogle Scholar
- Peakall, R., Smouse, P.E., 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 537–2539.Google Scholar
- Pertoldi, C., Hansen, M.M., Loeschke, V., Madsen, A.B., Jacobsen, L., Baagoe, H., 2001. Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993. Proc. R. Soc. B: Biol. Sci. 268, 1775–1781.CrossRefGoogle Scholar
- Ponnikas, S., Kvist, L., Ollila, T., Stjernberg, T., Orell, M., 2013. Genetic structure of an endangered raptor at individual and population levels. Conserv. Genet. 14 (6), 1135–1147.CrossRefGoogle Scholar
- Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
- Randi, E., 2011. Genetics and conservation of wolves Canis lupus in Europe. Mamm. Rev. 41, 99–111.CrossRefGoogle Scholar
- Randi, E., Davoli, F., Pierpaoli, M., Pertoldi, C., Madsen, A.B., Loeschke, V., 2003. Genetic structure in otter Lutra lutra populations in Europe: implications for conservation. Anim. Conserv. 6, 93–100.CrossRefGoogle Scholar
- Rannala, B., Mountain, J.L., 1997. Detecting immigration by using mulitlocus genotypes. Proc. Natl. Acad. Sci. U.S.A. 94 (17), 9197–9201.PubMedPubMedCentralCrossRefGoogle Scholar
- Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.CrossRefGoogle Scholar
- Roos, A.,Greyerz, E., Olsson, M., Sandegren, F., 2001. The Otter Lutra Lutra in Sweden-population Trends in Relation to Σ DDT and Total PCB Concentrations during 1968–1999. Environ. Pollut. 111 (3), 457–469.PubMedCrossRefPubMedCentralGoogle Scholar
- Roos, A., Bäcklin, B.-M., Helander, B., Rigét, F., Eriksson, U., 2012. Improved reproductive success in otters Lutra lutra, grey seals Halichoerus grypus and sea eagles Haliaeetus albicilla from Sweden in relation to concentrations of organochlorine contaminants. Environ. Pollut. 170, 268–275.PubMedCrossRefPubMedCentralGoogle Scholar
- Ruiz-Olmo, J., Loy, A., Cianfrani, C., Yoxon, P., Yoxon, G., de Silva, P.K., Roos, A., Bisther, M., Hajkova, P., Zemanova, B., 2008. Lutra lutra. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2, (https://doi.org/www.iucnredlist.org) (downloaded on 20.12.12).
- Schmidt, K., Ratkiewicz, M., Konopinski, M.K., 2011. The importance of genetic variability and population differentiation in the Eurasian lynx Lynx lynx for conservation, in the context of habitat and climate change. Mamm. Rev. 41, 112–124.CrossRefGoogle Scholar
- Sjöåsen, T., 1996. Surivorship of captivebred and wild-caught reintroduction European otters Lutra lutra in Sweden. Biol. Conser. 76, 161–165.CrossRefGoogle Scholar
- Sommer, R., Benecke, N., 2004. Late- and post-glacial history of the Mustelidae in Europe. Mamm. Rev. 34, 249–284.CrossRefGoogle Scholar
- Stanton, D.W.G., Hobbs, G.I., Chadwick, E.A., Slater, F.M., Bruford, M.W., 2009. Mitochondrial genetic diversity and structure of the European otter Lutra lutra in Britain. Conserv. Genet. 10, 733–737.CrossRefGoogle Scholar
- Stjernberg, T., Hagner-Wahlsten, N., 1994. Saukon levinneisyys Suomessa vuosina 1975 ja 1985 English summary: the distribution of the otter in Finland in 1975 and 1985. Suomen Riista 40, 42–49.Google Scholar
- Sulkava, R.T., Sulkava, P.O., Sulkava, P.E., 2007. Source and sink dynamics of density-dependent Otter Lutra lutra populations in rivers of central Finland. Oecologia 153, 579–588.PubMedCrossRefPubMedCentralGoogle Scholar
- Sulkava, R., Sulkava, P., 2009. Otter(Lutralutra) Population in Northernmost Finland. Est. J. Ecol. 58, 225–231.CrossRefGoogle Scholar
- Swenson, J.E.,Taberlet, P., Bellemain, E., 2011. Genetics and conservation of European brown bears Ursus arctos. Mamm. Rev. 41, 87–98.CrossRefGoogle Scholar
- Tiedemann, R., Harder, J., Gmeiner, C, Haase, E., 1996. Mitochondrial DNA sequence patterns of Harbour porpoises Phocoena phocoena from the North and the Baltic Sea. Z. Säugetierkd 61, 104–111.Google Scholar
- Tikhonov, A., Cavallini, P., Maran, T., Krantz, A., Herrero, J., Giannatos, G., Stubbe, M., Conroy, J., Krystufek, B., Abramov, A., Wozencraft, C, 2008. Vormela peregusna. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2, (https://doi.org/www.iucnredlist.org).
- Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4 (3), 535–538.CrossRefGoogle Scholar
- Villesen, P., 2007. FaBox: an online toolbox for fasta sequences. Mol. Ecol. Notes 7, 965–968.CrossRefGoogle Scholar
- Von Arx, M., Breitenmoser-Wursten, C., 2008. Lynx pardinus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2, (https://doi.org/www.iucnredlist.org) (downloaded on 20 December 2012).
- Zachos, F.E., Althoff, C., Steynitz, Y.v., Eckert, I., Hartl, G.B., 2007. Genetic analysis of an isolated red deer Cervus elaphus population showing signs of inbreeding depression. Eur. J. Wildlife Res. 53, 61–67.CrossRefGoogle Scholar