Skip to main content
SpringerLink
Log in

Population structure and recent temporal changes in genetic variation in Eurasian otters from Sweden

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The Eurasian otter (Lutra lutra) population in Sweden went through a drastic decline in population size between the 1950s and 1980s, caused mostly by anthropogenic factors such as high hunting pressure and the introduction of environmental toxic chemicals into the otter’s habitats. However, after the bans of PCBs and DDT in the 1970s, the population began to recover in the 1990s. This study compares microsatellite data across twelve loci from historical and contemporary otter samples to investigate whether there has been a change in population structure and genetic diversity across time in various locations throughout Sweden. The results suggest that otters in the south were more severely affected by the bottleneck, demonstrated by a decline in genetic diversity and a shift in genetic composition. In contrast, the genetic composition in otters from northern Sweden remained mostly unchanged, both in terms of population structure and diversity. This suggests that the decline was not uniform across the country. Moreover, our analyses of historical samples provide an overview of the level of genetic variation and population structure that existed prior to the bottleneck, which may be helpful for the future management and conservation of the species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aguilar A, Jessup DA, Estes J, Garza JC (2008) The distribution of nuclear genetic variation and historical demography of sea otters. Anim Conserv 11:35–45. doi:10.1111/j.1469-1795.2007.00144.x

    Article  Google Scholar 

  • Allendorf F, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Hoboken

    Google Scholar 

  • Allentoft ME et al (2011) Profiling the dead: generating microsatellite data from fossil bones of extinct megafauna-protocols, problems, and prospects. Plos One. doi:10.1371/journal.pone.0016670

    PubMed Central  PubMed  Google Scholar 

  • Arrendal J, Walker CW, Sundqvist AK, Hellborg L, Vila C (2004) Genetic evaluation of an otter translocation program. Conserv Genet 5:79–88. doi:10.1023/B:COGE.0000014059.49606.dd

    Article  CAS  Google Scholar 

  • Arrendal J, Vila C, Bjorklund M (2007) Reliability of noninvasive genetic census of otters compared to field censuses. Conserv Genet 8:1097–1107. doi:10.1007/s10592-006-9266-y

    Article  Google Scholar 

  • Bibby JC (1994) Recent past and future extinctions in birds. Philos Trans: Biol Sci 344:35–40

    Article  Google Scholar 

  • Bisther M, Roos A (2006) Uttern i Sverige 2006. Världsnaturfonden WWF, Rapport

  • Björklund M, Arrendal J (2008) Demo-genetic analysis of a recovering population of otters in central Sweden. Anim Conserv 11:529–534. doi:10.1111/j.1469-1795.2008.00214.x

    Article  Google Scholar 

  • Brace S et al (2012) Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability. Proc Nat Acad Sci USA 109:20532–20536. doi:10.1073/pnas.1213322109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cassens I, Tiedemann R, Suchentrunk F, Hartl GB (2000) Mitochondrial DNA variation in the European otter (Lutra lutra) and the use of spatial autocorrelation analysis in conservation. J Heredity 91:31–35

    Article  CAS  Google Scholar 

  • Cohen TM et al (2013) Genetic diversity of the Eurasian Otter (Lutra lutra) population in Israel. J Heredity 104:192–201. doi:10.1093/jhered/ess094

    Article  Google Scholar 

  • Colborn T (1991) Epidemiology of great-lakes bald eagles. J Toxicol Environ Health 33:395–453

    Article  CAS  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cornuet JM et al (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719. doi:10.1093/bioinformatics/btn514

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornuet JM et al (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics. doi: 10.1093/bioinformatics/btt763

  • Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol Ecol 7:1248–1251

    CAS  PubMed  Google Scholar 

  • Dallas JF et al (1999) Genetic diversity in the Eurasian otter, Lutra lutra, in Scotland. Evidence from microsatellite polymorphism. Biol J Linnean Soc 68:73–86. doi:10.1111/j.1095-8312.1999.tb01159.x

    Article  Google Scholar 

  • Dallas JF, Marshall F, Piertney SB, Bacon PJ, Racey PA (2002) Spatially restricted gene flow and reduced microsatellite polymorphism in the Eurasian otter Lutra lutra in Britain. Conserv Genet 3:15–29. doi:10.1023/A:1014259218632

    Article  CAS  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Nat Acad Sci 91:3166–3170. doi:10.1073/pnas.91.8.3166

    Article  PubMed Central  PubMed  Google Scholar 

  • Dunn OJ (1961) Multiple comparisons among means. J Am Statist Assoc 56:52. doi:10.2307/2282330

    Article  Google Scholar 

  • Eimes JA, Bollmer JL, Whittingham LA, Johnson JA, van Oosterhout C, Dunn PO (2011) Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J Evol Biol 24:1847–1856. doi:10.1111/j.1420-9101.2011.02311.x

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. doi:10.1038/nrg1348

    Article  CAS  PubMed  Google Scholar 

  • Erlinge S (1972) The situation of the otter population in Sweden. Viltrevy 8:337–397

    Google Scholar 

  • Erlinge S, Nilsson T (1978) Nedslående inventeringsresultat: uttern fortsätter att minska bara 1,000–1,500 uttrar kvar. Svensk Jakt 5:154–156

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ferrando A, Ponsa M, Marmi J, Domingo-Roura X (2004) Eurasian otters, Lutra lutra, have a dominant mtDNA haplotype from the Iberian Peninsula to Scandinavia. J Heredity 95:430–435. doi:10.1093/jhered/esh066

    Article  CAS  Google Scholar 

  • Foster-Turley P, Macdonald SM, Mason CF (1990) Otters: an action plan for their conservation. IUCN Species Survival Commission, Gland

  • Gagneux P, Boesch C, Woodruff DS (1997) Microsatellite scoring errors associated with noninvasive genotyping based on nuclear DNA amplified from shed hair. Mol Ecol 6:861–868. doi:10.1111/j.1365-294X.1997.tb00140.x

    Article  CAS  PubMed  Google Scholar 

  • Girod C, Vitalis R, Leblois R, Freville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188:165–179. doi:10.1534/genetics.110.121764

    Article  PubMed Central  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html (updated from Goudet 1995 citeulike-article-id: 7617994)

  • Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) Conservation biology—‘Ghost’ alleles of the Mauritius kestrel. Nature 403:616. doi:10.1038/35001148

    Article  CAS  PubMed  Google Scholar 

  • Guertin DA, Ben-David M, Harestad AS, Elliott JE (2012) Fecal genotyping reveals demographic variation in river otters inhabiting a contaminated environment. J Wildl Manage 76:1540–1550. doi:10.1002/Jwmg.439

    Article  Google Scholar 

  • Hailer F et al (2006) Bottlenecked but long-lived high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319. doi:10.1098/rsbl.2006.0453

    Article  PubMed Central  PubMed  Google Scholar 

  • Hajkova P, Pertoldi C, Zemanova B, Roche K, Hajek B, Bryja J, Zima J (2007) Genetic structure and evidence for recent population decline in Eurasian otter populations in the Czech and Slovak Republics: implications for conservation. J Zool 272:1–9. doi:10.1111/j.1469-7998.2006.00259.x

    Article  Google Scholar 

  • Harris CJ (1968) Otters: a study of the recent Lutrinae. Weidenfeld and Nicolson, London

    Google Scholar 

  • Heggberget TM (1988) Reproduction in the female European otter in central and northern Norway. J Mammal 69:164–167. doi:10.2307/1381766

    Article  Google Scholar 

  • Hobbs GI, Chadwick EA, Bruford MW, Slater FM (2011) Bayesian clustering techniques and progressive partitioning to identify population structuring within a recovering otter population in the UK. J Appl Ecol 48:1206–1217. doi:10.1111/j.1365-2664.2011.02028.x

    Article  Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21:797–807. doi:10.1007/s10980-005-5245-9

    Article  Google Scholar 

  • Honnen A-C, Petersen B, Kaßler L, Elmeros M, Roos A, Sommer RS, Zachos FE (2011) Genetic structure of Eurasian otter (Lutra lutra, carnivora: mustelidae) populations from the western Baltic sea region and its implications for the recolonization of north–western Germany. J Zool Systemat Evolut Res 49:169–175. doi:10.1111/j.1439-0469.2010.00582.x

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi: 10.1093/bioinformatics/btm233

  • Janssens X, Fontaine MC, Michaux JR, Libois R, de Kermabon J, Defourny P, Baret PV (2008) Genetic pattern of the recent recovery of European otters in southern France. Ecography 31:176–186. doi:10.1111/j.0906-7590.2008.4936.x

    Article  Google Scholar 

  • Johnson CJ, Hodder DP, Crowley S (2013) Assessing noninvasive hair and fecal sampling for monitoring the distribution and abundance of river otter. Ecol Res 28:881–892. doi:10.1007/s11284-013-1071-8

    Article  Google Scholar 

  • Kalz B, Jewgenow K, Fickel J (2006) Structure of an otter (Lutra lutra) population in Germany—results of DNA and hormone analyses from faecal samples. Mammalian Biol 71:321–335. doi:10.1016/j.mambrio.2006.02.010

    Google Scholar 

  • Ketmaier V, Bernardini C (2005) Structure of the mitochondrial control region of the Eurasian otter (Lutra lutra; carnivora, mustelidae): patterns of genetic heterogeneity and implications for conservation of the species in Italy. J Heredity 96:318–328. doi:10.1093/jhered/esi037

    Article  CAS  Google Scholar 

  • Kruuk H, Conroy JWH (1996) Concentrations of some organochlorines in otters (Lutra lutra L) in Scotland: implications for populations. Environ Pollut 92:165–171. doi:10.1016/0269-7491(95)00099-2

    Article  CAS  PubMed  Google Scholar 

  • Larson S, Jameson R, Bodkin J, Staedler M, Bentzen P (2002a) Microsatellite DNA and mitochondrial DNA variation in remnant and translocated sea otter (Enhydra lutris) populations. J Mammal 83:893–906. doi:10.1644/1545-1542(2002)083<0893:Mdamdv>2.0.Co;2

    Article  Google Scholar 

  • Larson S, Jameson R, Etnier M, Fleming M, Bentzen P (2002b) Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries. Mol Ecol 11:1899–1903

    Article  CAS  PubMed  Google Scholar 

  • Larson S, Monson D, Ballachey B, Jameson R, Wasser SK (2009) Stress-related hormones and genetic diversity in sea otters (Enhydra lutris). Mar Mammal Sci 25:351–372. doi: 10.1111/j.1748-7692.2008.00260.x

  • Larson S, Jameson R, Etnier M, Jones T, Hall R (2012) Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741–1911. PLoS One 7:e32205. doi:10.1371/journal.pone.0032205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larsson K, Ebenhard T (1994) Isolerade delpopulationer av utter: en sårbarhetsanalys. Världsnaturfonden WWF, Stockholm

    Google Scholar 

  • Mason CF (1993) PCB and organochlorine pesticide-residues in a sample of otter (Lutra lutra) spraints from northern-Ireland. Biol Environ 93B:111–112

  • Mason CF, Macdonald SM (1986) Otters: ecology and conservation. Cambridge University Press, Cambridge

    Google Scholar 

  • Mason CF, Macdonald SM (1994) PCBs and organochlorine pesticide residues in otters (Lutra lutra) and in otter spraints from SW England and their likely impact on populations. Sci Tot Environ 144:305–312

    Article  CAS  Google Scholar 

  • Mason CF, Madsen AB (1993) Organochlorine pesticide residues and PCBs in Danish otters (Lutra lutra). Sci Tot Environ 133:73–81

    Article  CAS  Google Scholar 

  • Mason CF, Ratford JR (1994) PCB congeners in tissues of European otter (Lutra lutra). Bull Environ Contamin Toxicol 53:548–554

    CAS  Google Scholar 

  • McMillan AM, Bagley MJ, Jackson SA, Nacci DE (2006) Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 15:539–548. doi:10.1007/s10646-006-0090-4

    Article  CAS  PubMed  Google Scholar 

  • Mucci N, Pertoldi C, Madsen AB, Loeschcke V, Randi E (1999) Extremely low mitochondrial DNA control-region sequence variation in the otter Lutra lutra population of Denmark. Hereditas 130:331–336

    Article  CAS  PubMed  Google Scholar 

  • Mucci N et al (2010) Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe. Conserv Genet 11:583–599. doi:10.1007/s10592-010-0054-3

    Article  Google Scholar 

  • Nacci DE, Champlin D, Jayaraman S (2010) Adaptation of the estuarine fish Fundulus heteroclitus (atlantic killifish) to polychlorinated biphenyls (PCBs). Estuar Coast 33:853–864. doi: 10.1007/s12237-009-9257-6

  • Nyström V, Angerbjörn A, Dalen L (2006) Genetic consequences of a demographic bottleneck in the Scandinavian arctic fox. Oikos 114:84–94. doi:10.1111/j.2006.0030-1299.14701.x

    Article  Google Scholar 

  • Nyström V et al (2012) Microsatellite genotyping reveals end-Pleistocene decline in mammoth autosomal genetic variation. Mol Ecol 21:3391–3402. doi:10.1111/j.1365-294X.2012.05525.x

    Article  PubMed  Google Scholar 

  • Oliver MK, Piertney SB (2012) Selection maintains MHC diversity through a natural population bottleneck. Mol Biol Evol 29:1713–1720. doi:10.1093/molbev/mss063

    Article  CAS  PubMed  Google Scholar 

  • Olsson M, Sandegren F (1983) The otter situation in Sweden and the Småland-Södermanland otter surveys of 1983. Paper presented at the the 3rd international otter symposium, Strasbourg, 24–27 November

  • Olsson M, Sandegren F (1986) Projekt Utter. Fauna och Flora 81:157–159

    Google Scholar 

  • Olsson M, Sandegren F (1991) Is PCB partly responsible for the decline of the otter in Europe? In: Reuther C, Röchert, R (ed) Proceedings of the V international otter colloquium, Hankens-bűttel, 1989, vol 6. Habitat, pp 223–227

  • Olsson M, Sandegren F, Rosendal E (1984) Utterinventering av delar av Ljusnans och Dalälvens avrinningsområden. Viltnytt 27:51–56

  • Olsson M, Sandegren F, Sjöåsen T (1988) Utterinventering, Norrland 1986–87. Rapport from the Swedish Natural History Museum and the Swedish Hunter Association to WWF, Statens naturvårdsverk och länsstyrelser

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peery MZ et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. doi:10.1111/j.1365-294X.2012.05635.x

    Article  PubMed  Google Scholar 

  • Perez-Haro M, Vinas J, Manas F, Batet A, Ruiz-Olmo J, Pla C (2005) Genetic variability in the complete mitochondrial control region of the Eurasian otter (Lutra lutra) in the Iberian Peninsula. Biol J Linn Soc 86:397–403. doi:10.1111/j.1095-8312.2005.00536.x

    Article  Google Scholar 

  • Pertoldi C, Hansen MM, Loeschcke V, Madsen AB, 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

    Article  CAS  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. doi:10.1038/sj.hdy.6800724

    CAS  PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Quaglietta L, Fonseca VC, Hajkova P, Mira A, Boitani L (2013) Fine-scale population genetic structure and short-range sex-biased dispersal in a solitary carnivore Lutra lutra. J Mammal 94:561–571. doi:10.1644/12-Mamm-a-171.1

    Article  Google Scholar 

  • Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544. doi:10.1016/j.biocon.2009.07.026

    Article  Google Scholar 

  • Raikkonen J, Bignert A, Mortensen P, Fernholm B (2006) Congenital defects in a highly inbred wild wolf population (Canis lupus). Mammalian Biology 71:65–73. doi:10.1016/j.mambio.2005.12.002

    Google Scholar 

  • Randi E, Davoli F, Pierpaoli M, Pertoldi C, Madsen AB, Loeschcke V (2003) Genetic structure in otter (Lutra lutra) populations in Europe: implications for conservation. Anim Conserv 6:93–100. doi: 10.1017/S1367943003123

  • Roark SA, Nacci D, Coiro L, Champlin D, Guttman SI (2005) Population genetic structure of a nonmigratory estuarine fish (Fundulus heteroclitus) across a strong gradient of polychlorinated biphenyl contamination. Environ Toxicol Chem 24:717–725

    Article  CAS  PubMed  Google Scholar 

  • Roos A, Greyerz E, Olsson M, Sandegren F (2001) The otter (Lutra lutra) in Sweden—population trends in relation to Sigma DDT and total PCB concentrations during 1968–1999. Environ Pollut 111:457–469. doi:10.1016/s0269-7491(00)00085-3

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x

    Article  Google Scholar 

  • Sandegren F, Olsson M (1989) Varför minskar uttern? Svensk Jakt 2:86–90

  • Santos EM, Hamilton PB, Coe TS, Ball JS, Cook AC, Katsiadaki I, Tyler CR (2013) Population bottlenecks, genetic diversity and breeding ability of the three-spined stickleback (Gasterosteus aculeatus) from three polluted English rivers. Aquat Toxicol 142:264–271. doi:10.1016/j.aquatox.2013.08.008

    Article  PubMed  Google Scholar 

  • Sjöåsen T (1996) Survivorship of captive-bred and wild-caught reintroduced European otters Lutra lutra in Sweden. Biol Conserv 76:161–165

    Article  Google Scholar 

  • Smit MD, Leonards PE, de Jongh AW, van Hattum BG (1998) Polychlorinated biphenyls in the Eurasian otter (Lutra lutra). Rev Environ Contam Toxicol 157:95–130

    CAS  PubMed  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573. doi:10.1038/sj.hdy.6885180

    Article  PubMed  Google Scholar 

  • Stanton DWG, Hobbs GI, Chadwick EA, Slater FM, Bruford MW (2009) Mitochondrial genetic diversity and structure of the European otter (Lutra lutra) in Britain. Conserv Genet 10:733–737. doi:10.1007/s10592-008-9633-y

    Article  CAS  Google Scholar 

  • Stanton DWG et al (2014) Contrasting genetic structure of the Eurasian otter (Lutra lutra) across a latitudinal divide. J Mammal 95:814–823. doi:10.1644/13-MAMM-A-201

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. doi:10.1126/science.1103538

    Article  CAS  PubMed  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203. doi:10.1016/s0169-5347(00)01825-5

    Article  PubMed  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. doi: 10.1093/bioinformatics/btn478

  • Taberlet P, Luikart G (1999) Non-invasive genetic sampling and individual identification. Biol J Linn Soc 68:41–55. doi:10.1111/j.1095-8312.1999.tb01157.x

    Article  Google Scholar 

  • Takezaki N, Nei M, Tamura K (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with windows interface. Mol Biol Evol 27:747–752. doi:10.1093/molbev/msp312

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vos JG et al (2000) Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit Rev Toxicol 30:71–133. doi:10.1080/10408440091159176

    Article  CAS  PubMed  Google Scholar 

  • Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642. doi:10.1016/j.tree.2007.08.017

    Article  PubMed  Google Scholar 

  • Wirgin I, Waldman JR (2004) Resistance to contaminants in north American fish populations. Mutat Res Fund Mol M 552:73–100. doi:10.1016/j.mrfmmm.2004.06.005

    Article  CAS  Google Scholar 

  • Woodroffe R (2000) Predators and people: using human densities to interpret declines of large carnivores. Anim Conserv 3:165–173. doi:10.1111/j.1469-1795.2000.tb00241.x

    Article  Google Scholar 

  • Yang DY, Eng B, Waye JS, Dudar JC, Saunders SR (1998) Technical note: improved DNA extraction from ancient bones using silica-based spin columns. Am J Phys Anthropol 105:539–543. doi:10.1002/(sici)1096-8644(199804)105:4<539:aid-ajpa10>3.0.co;2-1

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Daniela Kalthoff (Swedish Museum of Natural History, Stockholm) and Friederike Johansson (Göteborg Museum of Natural History) for providing the museum samples for the DNA analysis. We also thank Nils Ryman, Olle Karlsson and Ulf Jondelius for comments on an earlier version of the manuscript. This work was supported by a grant from the Swedish Research Council to LD.

Conflict of interest

The authors have no conflicts of interest to declare.

Author information

Authors and Affiliations

  1. Department of Bioinformatics and Genetics, Swedish Museum of Natural History, SE-10405, Stockholm, Sweden

    Jean-Luc Tison, Victor Blennow, Eleftheria Palkopoulou, Petra Gustafsson & Love Dalén

  2. Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, SE-10691, Stockholm, Sweden

    Jean-Luc Tison

  3. Department of Zoology, Stockholm University, SE-10691, Stockholm, Sweden

    Victor Blennow, Eleftheria Palkopoulou & Petra Gustafsson

  4. Department of Environmental Research and Monitoring, Swedish Museum of Natural History, SE-10405, Stockholm, Sweden

    Anna Roos

Authors
  1. Jean-Luc Tison
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Victor Blennow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eleftheria Palkopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Petra Gustafsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna Roos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Love Dalén
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Luc Tison.

Additional information

Jean-Luc Tison and Victor Blennow have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1,143 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tison, JL., Blennow, V., Palkopoulou, E. et al. Population structure and recent temporal changes in genetic variation in Eurasian otters from Sweden. Conserv Genet 16, 371–384 (2015). https://doi.org/10.1007/s10592-014-0664-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0664-2

Keywords

Search

Navigation