Skip to main content

Advertisement

Log in

Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe

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

Abstract

Eurasian otter populations strongly declined and partially disappeared due to global and local causes (habitat destruction, water pollution, human persecution) in parts of their continental range. Conservation strategies, based on reintroduction projects or restoration of dispersal corridors, should rely on sound knowledge of the historical or recent consequences of population genetic structuring. Here we present the results of a survey performed on 616 samples, collected from 19 European countries, genotyped at the mtDNA control-region and 11 autosomal microsatellites. The mtDNA variability was low (nucleotide diversity = 0.0014; average number of pairwise differences = 2.25), suggesting that extant otter mtDNA lineages originated recently. A star-shaped mtDNA network did not allow outlining any phylogeographic inference. Microsatellites were only moderately variable (H o = 0.50; H e = 0.58, on average across populations), the average allele number was low (observed A o = 4.9, range 2.5–6.8; effective A e = 2.8; range 1.6–3.7), suggesting small historical effective population size. Extant otters likely originated from the expansion of a single refugial population. Bayesian clustering and landscape genetic analyses however indicate that local populations are genetically differentiated, perhaps as consequence of post-glacial demographic fluctuations and recent isolation. These results delineate a framework that should be used for implementing conservation programs in Europe, particularly if they are based on the reintroduction of wild or captive-reproduced otters.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arrendal J, Walker CW, Sundqvist AK et al (2004) Genetic evaluation of an otter translocation program. Conserv Genet 5:79–88

    Article  CAS  Google Scholar 

  • Avise JC (1986) Mitochondrial DNA and evolutionary genetics of higher animals. Phil Trans R Soc Lond B 312:325–342

    Article  CAS  Google Scholar 

  • Bandelt HL, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  • Beaumont M (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    CAS  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L et al. (2001) Genetix 4.02, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France. http://www.genetix.univ-montp2.fr/genetix/genetix.htm

  • Benzecri JP (1973) L’Analyse des donnees. Vol 2, L’Analyse des correspondances. Dunod, Paris

    Google Scholar 

  • Bifolchi A, Lodè T (2005) Efficiency of conservation shortcuts: an investigation with otters as umbrella species. Biol Conserv 126:523–527

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol Ecol 7:1247–1251

    Article  Google Scholar 

  • Dallas JF, Bacon PJ, Carss DN et al (1999) Genetic diversity in the Eurasian otter, Lutra lutra, in Scotland. Evidence from microsatellite polymorphism. Biol J Linn Soc 68:73–86

    Article  Google Scholar 

  • Dallas JF, Marshall F, Piertney SB et al (2002) Spatially restricted gene flow and reduced microsatellite polymorphism in the Eurasian otter Lutra lutra in Britain. Conserv Genet 3:15–29

    Article  CAS  Google Scholar 

  • Durbin LS (1996) Individual differences in spatial utilization of a river system by otters Lutra lutra. Acta Theriol 41:137–147

    Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Effenberger S, Suchentrunk F (1999) RFLP analysis of mitochondrial DNA of otters (Lutra lutra) from Europe. Implications for the conservation of a flagship species. Biol Conserv 90:229–234

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolut Bioinform Online 1:47–50

    CAS  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

    CAS  PubMed  Google Scholar 

  • Ferrando A, Ponsà M, Marmi J, Domingo-Roura X (2004) Eurasian otters, Lutra lutra, have a dominant mtDNA haplotype from the Iberian Peninsula to Scandinavia. J Hered 95:430–435

    Article  CAS  PubMed  Google Scholar 

  • Finnegan LA, Néill LÓ (2009) Mitochondrial DNA diversity of the Irish otter, Lutra lutra, population. Conserv Genet. doi:10.1007/s10592-009-9955-4

  • Fiore I, Gala M, Tagliacozzo A (2004) Ecology and subsistence strategies in the eastern Italian Alps during the Middle Palaeolithic. Int J Osteoarchaeol 14:273–286

    Article  Google Scholar 

  • Foster-Turley P, Santiapillai C (1990) Action plan for Asian otters. In: Foster-Turley P, Macdonald SM, Mason CF (eds) Otters: an action plan for their conservation. IUCN, Gland, Switzerland

    Google Scholar 

  • Garnier S, Alibert P, Audiot P et al (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus somieri. Mol Ecol 13:1883–1897

    Article  CAS  PubMed  Google Scholar 

  • Gerloff U, Schlotterer C, Rassmann K et al (1995) Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living Bonobos (Pan paniscus). Mol Ecol 4:515–518

    Article  CAS  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Hajkova P, Pertoldi C, Zemanova B et al (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

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • IUCN (1998) Guidelines for re-introductions. Prepared by the IUCN/SSC re-introduction specialist group. IUCN, Gland and Cambridge

    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

    Article  CAS  PubMed  Google Scholar 

  • Jansman HAH, Chanin PRF, Dallas JF (2001) Monitoring otter populations by DNA typing of spraints. IUCN Otter Spec Group Bull 18:12–19

    Google Scholar 

  • Janssens X, Fontaine MC, Michaux JR et al (2008) Genetic pattern of the recent recovery of European otters in southern France. Ecography 31(2):176–186

    Article  Google Scholar 

  • Jefferies DJ, Wayre P, Jessop RM, Mitchell-Jones AJ (1986) Reinforcing the native otter Lutra lutra population in East Anglia: an analysis of the behavior and range development of the first release group. Mamm Rev 16:65–79

    Article  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 Hered 96:318–328

    Article  CAS  PubMed  Google Scholar 

  • Ki JS, Hwang DS, Park TJ et al (2009) A comparative analysis of the complete mitochondrial genome of the Eurasian otter, Lutra lutra (Carnivora; Mustelidae) Mol Biol Rep. doi:10.1007/s11033-009-9641-0

  • Koelewijn HP, Jansman HAH (2007) The Dutch otter reintroduction project: what non-invasive genetic sampling told us about social structure and behaviour in a low density population. In: Proceedings of V European congress of mammalogy, Siena, Italy. Hystrix It J Mamm, 2:524, 21–26 September 2007

  • Koepfli KP, Wayne RK (1998) Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial Cytochrome b sequences. J Zool 246:401–416

    Article  Google Scholar 

  • Koepfli KP, Kanchanasaka B, Sasaki H, Jacques H, Louie KDY, Hoai T, Xuan Dang N, Geffen E, Gutleb A, Han S, Heggberget TM, Lionel LaFontaine L, Lee H, Roland Melisch R, Ruiz-Olmo J, Santos-Reis M, Sidorovich VE, Stubbe M, Wayne RK (2008) Establishing the foundation for an applied molecular taxonomy of otters in Southeast Asia. Conserv Genet 9:1589–1604

    Article  Google Scholar 

  • Kruuk H (2006) Otters ecology, behaviour and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Occasional Papers, Museum of Texas Tech University 163:1–4

    Google Scholar 

  • Macdonald SM, Mason CF (1994) Status and conservation needs of the otter (Lutra lutra) in the western Palaearctic. Nat Environ 67:1–54

    Google Scholar 

  • Madsen AB (1996) Otter (Lutra lutra) mortality in relation to traffic and experience with using stop-grids in Denmark. In: Proceedings of the Vth International Otter Colloquium. Habitat 6:237–241

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:273–375

    Article  Google Scholar 

  • Mucci N, Pertoldi C, Madsen AB et al (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 

  • Musiani M, Leonard JA, Cluff HD et al (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. Mol Ecol 16:4149–4170

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burdens M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pérez-Haro M, Viñas J, Mañas F et al (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

    Article  Google Scholar 

  • Pertoldi C, Hansen MM, Loeschcke V et al (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 Lond B Biol Sci 268:1775–1781

    Article  CAS  Google Scholar 

  • Prigioni C, Remonti L, Balestrieri A et al (2006) Estimation of European otter (Lutra lutra) population size by fecal DNA typing in southern Italy. J Mammal 87:855–858

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Randi E, Davoli F, Pierpaoli M et al (2003) Genetic structure in otter (Lutra lutra) populations in Europe: implications for conservation. Anim Conserv 6:1–10

    Article  Google Scholar 

  • Randi E, Mucci N, Arrendal J et al (2005) Assessing the patterns of genetic diversity in otter populations in Europe. In: European Otter Workshop, Padula (Salerno), Italy, 20–23 October 2005

  • Reuther C (1994) European otter habitat network. In: Seminar on the conservation of the European otter (Lutra lutra), Environmental Encounters 24, Strasbourg, Leeuwarden, Council of Europe

  • Reuther C, Roy A (2001) Some results of the 1991 and 1999 otter (Lutra lutra) surveys in the River Ise catchment, Lower-Saxony, Germany. IUCN Otter Spec Group Bull 18:28–40

    Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC et al (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Olmo J, López-Martín JM, Palazón S (2001) The influence of fish abundance on the otter (Lutra lutra) populations in Iberian Mediterranean habitats. J Zool 254:325–336

    Article  Google Scholar 

  • Saavedra D, Sargatal J (1998) Reintroduction of the otter (Lutra lutra) in northeast Spain (Girona Province). Galemys 10:191–199

    Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites. Application to human mitochondrial DNA. Genetics 152:1079–1089

    CAS  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 

  • Sommer R, Benecke N (2004) Late- and Post-Glacial history of the Mustelidae in Europe. Mamm Rev 34:249–284

    Article  Google Scholar 

  • Sommer RS, Nadachowski A (2006) Glacial refugia of mammals in Europe: evidence from fossil records. Mamm Rev 36:251–265

    Article  Google Scholar 

  • Stanton DWG, Hobbs GI, Chadwick EA et al (2009) Mitochondrial genetic diversity and structure of the European otter (Lutra lutra) in Britain. Cons Genet 10:733–737

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  Google Scholar 

  • Van Ewijk KY, Knol AP, De Jong RCCM (1997) An otter PVA as a preparation of a reintroduction experiment in the Netherlands. Z Saugetier 62:238–242

    Google Scholar 

  • Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106

    Article  Google Scholar 

  • Wayre J (1991) The Otter Trust’s reintroduction programme using captive-bred otters. In: Reuther C, Rochert C, Hankensbiattel R (eds) Proceedings of international Otter Colloquium. Habitat 6:219–222

  • Weber D, Weber JM, Müller HU (1991) Fischotter (Lutra lutra L.) in Schwarzwasser-sensegebiet; dokumentation eines gescheiterten Wiedereinbürgerungsversuches. [Otters in the Schwarzwasser-Sense-catchment; documentation of an unsuccessful re-introduction project.] Mitteilungen der Naturforschenden Gesellschaft in Bern. (In German with English summary)

  • Wright S (1969) Evolution and the genetics of populations. Vol 2, the theory of gene frequencies. University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

This study has been partly supported by the Italian Ministry of Environment, Department of Nature Conservation. We wish to thank the ConGen program (funded by the European Science Foundation) and the Danish Natural Science Research Council for financial support to C. Pertoldi (grant number: #21-01-0526, #21-03-0125 and 95095995). P. Hajkova was supported by the Grant Agency of the Academy of Sciences of the Czech Republic, grant no. KJB600930804 and by the Ministry of the Environment of the Czech Republic, grant no. VaV-SP/2d4/16/08. VaV-SP/2d4/16/08. We thank everybody who helped in sampling collection. In particular, for France, L. Lafontaine wishes to acknowledge all people who provided otter samples for this study, and/or belonging to the following networks : SFEPM, LPO, ONCFS (DRD CNERA-PAD, F. Léger, P. Migot, D. Serre), ONEMA, FDAPPMA, Parcs Naturels Régionaux de Brière (X. Moyon), du Morvan, MNHN (G. Véron) and Muséums d’Histoire Naturelle of La Rochelle, Orléans, Toulouse, ENV Nantes, ADEV, GMB, Syndicat du Bassin du Scorff, Station INRA Moulin des Princes, APPMA Plouay, Base du Douron, EDENN, AREMIP, LPO Marais Breton, Fédérations Départementales des Chasseurs and officers from the Office National de la Chasse et de la Faune Sauvage SD12, SD17, SD22, SD29, SD33, SD35, SD40, SD44, SD56, SD85. The careful revisions done by three anonymous referees, and additional comments by the Associated Editor, greatly aided us to improve early versions of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ettore Randi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-010-0054-3

Keywords

Navigation