Conservation Genetics

, Volume 16, Issue 2, pp 371–384 | Cite as

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

  • Jean-Luc Tison
  • Victor Blennow
  • Eleftheria Palkopoulou
  • Petra Gustafsson
  • Anna Roos
  • Love Dalén
Research Article

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.

Keywords

Lutra lutra Microsatellites Population structure Bottleneck Coalescent simulations 

Supplementary material

10592_2014_664_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1,143 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. Allendorf F, Luikart G (2007) Conservation and the genetics of populations. Blackwell, HobokenGoogle Scholar
  3. 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 PubMedCentralPubMedGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. Bibby JC (1994) Recent past and future extinctions in birds. Philos Trans: Biol Sci 344:35–40CrossRefGoogle Scholar
  7. Bisther M, Roos A (2006) Uttern i Sverige 2006. Världsnaturfonden WWF, RapportGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  10. 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 91:31–35CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. Colborn T (1991) Epidemiology of great-lakes bald eagles. J Toxicol Environ Health 33:395–453CrossRefPubMedGoogle Scholar
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedCentralPubMedGoogle Scholar
  14. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  15. 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
  16. Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol Ecol 7:1248–1251PubMedGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Dunn OJ (1961) Multiple comparisons among means. J Am Statist Assoc 56:52. doi:10.2307/2282330 CrossRefGoogle Scholar
  21. 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 CrossRefPubMedGoogle Scholar
  22. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. doi:10.1038/nrg1348 CrossRefPubMedGoogle Scholar
  23. Erlinge S (1972) The situation of the otter population in Sweden. Viltrevy 8:337–397Google Scholar
  24. Erlinge S, Nilsson T (1978) Nedslående inventeringsresultat: uttern fortsätter att minska bara 1,000–1,500 uttrar kvar. Svensk Jakt 5:154–156Google Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. Foster-Turley P, Macdonald SM, Mason CF (1990) Otters: an action plan for their conservation. IUCN Species Survival Commission, GlandGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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)
  32. Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) Conservation biology—‘Ghost’ alleles of the Mauritius kestrel. Nature 403:616. doi:10.1038/35001148 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. Harris CJ (1968) Otters: a study of the recent Lutrinae. Weidenfeld and Nicolson, LondonGoogle Scholar
  37. Heggberget TM (1988) Reproduction in the female European otter in central and northern Norway. J Mammal 69:164–167. doi:10.2307/1381766 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 11:1899–1903CrossRefPubMedGoogle Scholar
  49. 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
  50. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  51. Larsson K, Ebenhard T (1994) Isolerade delpopulationer av utter: en sårbarhetsanalys. Världsnaturfonden WWF, StockholmGoogle Scholar
  52. Mason CF (1993) PCB and organochlorine pesticide-residues in a sample of otter (Lutra lutra) spraints from northern-Ireland. Biol Environ 93B:111–112Google Scholar
  53. Mason CF, Macdonald SM (1986) Otters: ecology and conservation. Cambridge University Press, CambridgeGoogle Scholar
  54. 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 144:305–312CrossRefGoogle Scholar
  55. Mason CF, Madsen AB (1993) Organochlorine pesticide residues and PCBs in Danish otters (Lutra lutra). Sci Tot Environ 133:73–81CrossRefGoogle Scholar
  56. Mason CF, Ratford JR (1994) PCB congeners in tissues of European otter (Lutra lutra). Bull Environ Contamin Toxicol 53:548–554Google Scholar
  57. 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 CrossRefPubMedGoogle Scholar
  58. 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 130:331–336CrossRefPubMedGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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
  61. 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 CrossRefGoogle Scholar
  62. 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 CrossRefPubMedGoogle Scholar
  63. 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 CrossRefPubMedGoogle Scholar
  64. 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 NovemberGoogle Scholar
  65. Olsson M, Sandegren F (1986) Projekt Utter. Fauna och Flora 81:157–159Google Scholar
  66. 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 223–227Google Scholar
  67. Olsson M, Sandegren F, Rosendal E (1984) Utterinventering av delar av Ljusnans och Dalälvens avrinningsområden. Viltnytt 27:51–56Google Scholar
  68. 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 länsstyrelserGoogle Scholar
  69. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  70. 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 CrossRefPubMedGoogle Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 268:1775–1781CrossRefGoogle Scholar
  73. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. doi:10.1038/sj.hdy.6800724 PubMedGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  76. 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 CrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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
  79. 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
  80. 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 24:717–725CrossRefPubMedGoogle Scholar
  81. 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 CrossRefPubMedGoogle Scholar
  82. 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 CrossRefGoogle Scholar
  83. Sandegren F, Olsson M (1989) Varför minskar uttern? Svensk Jakt 2:86–90Google Scholar
  84. 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 CrossRefPubMedGoogle Scholar
  85. Sjöåsen T (1996) Survivorship of captive-bred and wild-caught reintroduced European otters Lutra lutra in Sweden. Biol Conserv 76:161–165CrossRefGoogle Scholar
  86. Smit MD, Leonards PE, de Jongh AW, van Hattum BG (1998) Polychlorinated biphenyls in the Eurasian otter (Lutra lutra). Rev Environ Contam Toxicol 157:95–130PubMedGoogle Scholar
  87. 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 CrossRefPubMedGoogle Scholar
  88. 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 CrossRefGoogle Scholar
  89. 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 CrossRefGoogle Scholar
  90. 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 CrossRefPubMedGoogle Scholar
  91. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203. doi:10.1016/s0169-5347(00)01825-5 CrossRefPubMedGoogle Scholar
  92. 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
  93. 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 CrossRefGoogle Scholar
  94. 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 CrossRefPubMedCentralPubMedGoogle Scholar
  95. 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 CrossRefPubMedGoogle Scholar
  96. 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 CrossRefPubMedGoogle Scholar
  97. 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 CrossRefGoogle Scholar
  98. 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 CrossRefGoogle Scholar
  99. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Jean-Luc Tison
    • 1
    • 2
  • Victor Blennow
    • 1
    • 3
  • Eleftheria Palkopoulou
    • 1
    • 3
  • Petra Gustafsson
    • 1
    • 3
  • Anna Roos
    • 4
  • Love Dalén
    • 1
  1. 1.Department of Bioinformatics and GeneticsSwedish Museum of Natural HistoryStockholmSweden
  2. 2.Department of Molecular BiosciencesThe Wenner-Gren Institute, Stockholm UniversityStockholmSweden
  3. 3.Department of ZoologyStockholm UniversityStockholmSweden
  4. 4.Department of Environmental Research and MonitoringSwedish Museum of Natural HistoryStockholmSweden

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