Skip to main content

Advertisement

Log in

MHC class II variation in the endangered European mink Mustela lutreola (L. 1761)—consequences for species conservation

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The polymorphic major histocompatibility complex (MHC) has gained a specific relevance in pathogen resistance and mate choice. Particularly the antigen-binding site (ABS), encoded by exon 2 of the DRB class II gene, exhibits numerous alleles and extensive sequence variations between alleles. A lack of MHC variability has attributed to instances such as bottleneck effects or relaxed selection pressure and has a certain impact on the long-term viability of the species concerned. As a result of seriously decreased population density during the last century, the current population of the endangered European mink (Mustela lutreola, L. 1761) has suffered from geographic isolation. In this study, we amplified a partial sequence of the MHC class II DRB exon 2 (229 bp), assessed the degree of genetic variation and compared the variability with those of other Mustelidae. As a result, nine alleles were detected in 20 investigated individuals, which differ from each other by four to 25 nucleotide substitutions (two to 11 amino acid substitutions). Whilst an equal ratio for synonymous and non-synonymous substitutions was found inside the ABS, synonymous substitutions were significantly higher than non-synonymous substitutions in the non-ABS region. Results might indicate that no positive selection exists within the ex situ population of M. lutreola, at least in the analysed fragment. In addition, phylogenetic analyses support the trans-species model of evolution.

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

Similar content being viewed by others

References

  • Abramov AV (2000) A taxonomic review of the genus Mustela (Mammalia, Carnivora). Zoosyst Ross 8:357–364

    Google Scholar 

  • Aguilar A, Roemer G, Debenham S et al (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494 doi:10.1073/pnas.0306582101

    Article  PubMed  CAS  Google Scholar 

  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17(2):179–224

    PubMed  CAS  Google Scholar 

  • 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 doi:10.1111/j.1365-294X.2005.02605.x

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp GK, Yamazaki K (2005) Individual differences and the chemical senses. Chem Senses 30(1):i6–i9 doi:10.1093/chemse/bjh086

    Article  PubMed  Google Scholar 

  • Bowen L, Aldridge BM, Gulland F et al (2002) Molecular characterization of expressed DQA and DQB genes in the California sea lion (Zalophus californianus). Immunogenetics 54:332–347 doi:10.1007/s00251-002-0472-6

    Article  PubMed  CAS  Google Scholar 

  • Brown JH, Jardetzky TS, Gorga JC et al (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39

    Article  PubMed  CAS  Google Scholar 

  • Cabria MT, González EG, Gómez-Moliner BJ, Zardoya R (2007) Microsatellite markers for the endangered European mink (Mustela lutreola) and closely related mustelids. Mol Ecol Notes 7(6):1185–1188 doi:10.1111/j.1471-8286.2007.01825.x

    Article  CAS  Google Scholar 

  • Dyall R, Messaoudi I, Janetzki S, Nikolić-Žugić J (2000) MHC polymorphism can enrich the T cell repertoire of the species by shifts in intrathymic selection. J Immunol 164:1695–1698

    PubMed  CAS  Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311 doi:10.1016/S0169-5347(98)01416-5

    Article  Google Scholar 

  • Erlich HA, Bugawan TL (1990) HLA DNA typing. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. A guide to methods and applications. Academic, New York, pp 261–271

    Google Scholar 

  • 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 USA 90(17):8150–8153 doi:10.1073/pnas.90.17.8150

    Article  PubMed  CAS  Google Scholar 

  • Garza JC (1998) Population genetics in the Northern elephant seal. Unpublished thesis, University of California, Berkeley

  • Gilpin M, Wills C (1991) MHC and captive breeding: a rebuttal. Conserv Biol 5(4):554–555 doi:10.1111/j.1523-1739.1991.tb00368.x

    Article  Google Scholar 

  • Groombridge B (1994) 1994 IUCN red list of threatened animals. IUCN, Gland, Switzerland

    Google Scholar 

  • Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964 doi:10.1086/285643

    Article  Google Scholar 

  • Hedrick PW, Kim TJ (2000) Genetics of complex polymorphism: parasites and maintenance of the major histocompatibility complex variation. In: Singh RS, Krimbas CB (eds) Evolutionary genetics: from molecules to morphology. Cambridge University Press, Cambridge, pp 204–234

    Google Scholar 

  • Hedrick PW, Parker KM, Miller EL, Miller PS (1999) Major histocompatibility complex variation in the endangered Przewalski’s horse. Genetics 152:1701–1710

    PubMed  CAS  Google Scholar 

  • Hedrick PW, Parker KM, Gutiérrez-Espeleta GA, Rattink A, Lievers K (2000a) Major histocompatibility complex variation in the Arabian oryx. Evolution 54(6):2145–2151

    PubMed  CAS  Google Scholar 

  • Hedrick PW, Lee RN, Parker KM (2000b) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity 85:617–624

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL (1991) MHC polymorphism and the design of captive breeding programs. Conserv Biol 5:249–250

    Article  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Google Scholar 

  • Kavaliers M, Colwell DD (1992) Aversive responses of female mice to the odors of parasitized males: neuromodulatory mechanisms and implications for mate choice. Ethology 95:202–212

    Article  Google Scholar 

  • Kavaliers M, Colwell DD (1995a) Odors of oarasitized males induce aversive responses in female mice. Anim Behav 50:1161–1169

    Article  Google Scholar 

  • Kavaliers M, Colwell DD (1995b) Discrimination by female mice between the odors of parasitized and non-parasitized males. Proc R Soc Lond B Biol Sci 261(1360):31–35

    Article  CAS  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162

    Article  PubMed  CAS  Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL et al (1990) Nomenclature for the major histocompatibility complexes of different species, a proposal. Immunogenetics 31:217–219

    PubMed  CAS  Google Scholar 

  • L’Abbe D, Belmaaza A, Décary F, Chartrand P (1992) Elimination of heteroduplex artifacts when sequencing HLA genes amplified by polymerase chain reaction (PCR). Immunogenetics 35:395–397

    PubMed  Google Scholar 

  • Lafferty KD, Gerber L (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv Biol 16:593–604

    Article  Google Scholar 

  • Laurenson K, Sillero-Zubiri C, Thompson H et al (1998) Disease as a threat to endangered species: Ethiopian wolves, domestic dogs and canine pathogens. Anim Conserv 1:273–280

    Article  Google Scholar 

  • Lodé T (1999) Genetic bottleneck in the threatened western population of European mink Mustela lutreola. Ital J Zool (Modena) 66(4):351–353

    Article  Google Scholar 

  • Lyles AM, Dobson AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wildl Med 24:315–326

    Google Scholar 

  • Maran T, Henttonen H (1995) Why is the European mink (Mustela lutreola) disappearing?—A review of the process and hypotheses. Ann Zool Fenn 32:47–54

    Google Scholar 

  • Maran T, Polma M (2003) Reproduction of the European mink, Mustela lutreola, in captivity. Poster, International Conference on the Conservation of the European Mink, La Rioja, Spain, 5–8 November

  • Markov AV, Kulikov AM (2006) The hypothesis of immune testing of partners—coordinated adaptations and changes in mating preferences. Izv Akad Nauk Ser Biol (3):261–274

    PubMed  Google Scholar 

  • Messaoudi I, Guevara Patiňo JA, Dyall R, LeMaoult J, Nikolich-Žugich J (2002) Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 298:1797–1800

    Article  PubMed  CAS  Google Scholar 

  • Meyerhans A, Vartanian JP, Wain-Hobson S (1990) DNA recombination during PCR. Nucleic Acids Res 18(7):1687–1691

    Article  PubMed  CAS  Google Scholar 

  • Michaux JR, Libois R, Davison A, Chevret P, Rosoux R (2004) Is the western population of the European mink, (Mustela lutreola), a distinct management unit for conservation? Biol Conserv 115:357–367

    Article  Google Scholar 

  • Michaux JR, Hardy OJ, Justy F et al (2005) Conservation genetics and population history of the threatened European mink Mustela lutreola, with an emphasis on the west European population. Mol Ecol 14:2373–2388

    Article  PubMed  CAS  Google Scholar 

  • Mikko S, Andersson L (1995) Low major histocompatibility complex class II diversity in European and North American moose. Proc Natl Acad Sci USA 92:4259–4263

    Article  PubMed  CAS  Google Scholar 

  • Mikko S, Spencer M, Morris B et al (1997) A comparative analysis of Mhc DRB3 polymorphism in the American bison (Bison bison). J Hered 88:499–503

    PubMed  CAS  Google Scholar 

  • Mikko S, Røed K, Schmutz S, Andersson L (1999) Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants. Immunol Rev 167:169–178

    Article  PubMed  CAS  Google Scholar 

  • Miller SP, Hedrick PW (1991) MHC polymorphism and the design of captive breeding programs: simple solutions are not the answer. Conserv Biol 5(4):556–558

    Article  Google Scholar 

  • Murray DL, Kapke CA, Evermann JF, Fuller TK (1999) Infectious disease and the conservation of free-ranging large carnivores. Anim Conserv 2:241–254

    Article  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitution. Mol Biol Evol 3:418–426

    PubMed  CAS  Google Scholar 

  • O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259

    Article  Google Scholar 

  • Peltier D, Lodé T (2003) Molecular survey of genetic diversity in the endangered European mink Mustela lutreola. C R Biol 325:49–53 doi:10.1016/S1631-0691(03)00037-4

    Article  CAS  Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153(2):145–164

    Article  Google Scholar 

  • Potts WK (2002) Wisdom through immunogenetics. Nat Genet 30:130–131

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio J, Messenguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2469–2497

    Article  CAS  Google Scholar 

  • Seddon B (1999) Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Mol Ecol 8:2071–2079 doi:10.1046/j.1365-294x.1999.00822.x

    Article  PubMed  CAS  Google Scholar 

  • Smulders MJM, Snœk LB, Booy G, Vosman B (2003) Complete loss of MHC genetic diversity in the common hamster (Cricetus cricetus) population in The Netherlands. Consequences for conservation strategies. Conservation Genetics 4:441–451

    Article  CAS  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2(16):1–18

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA4) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Vrijenhoek RC, Leberg PL (1991) Let’s not throw the baby out with the bathwater: a comment on management for MHC diversity in captive populations. Conserv Biol 5:252–254

    Article  Google Scholar 

  • Wagner JL, Burnett RC, Works JD, Storb R (1996) Molecular analysis of DLA-DRBB1 polymorphism. Tissue Antigens 48:554–561

    Article  PubMed  CAS  Google Scholar 

  • Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol 13:711–718 doi:10.1111/j.1365-294X.2004.02095.x

    Article  PubMed  CAS  Google Scholar 

  • Wedekind C, Seebeck T, Bettens F, Paepke A (1995) MHC-dependent mate preferences in humans. Proc R Soc Lond B Biol Sci 260:245–249

    Article  CAS  Google Scholar 

  • Wibbelt G, Speck S, Frölich K, Peters E, Seebass C (2006) Causes of mortality in a European mink EEP breeding colony. VII. Conference of the European Wildlife Diseases Association, 27–30 September, Aosta Valley, Italy

Download references

Acknowledgements

We express our gratitude to W. Festl (EuroNerz e.V.) for the logistic support and for providing samples. Special thanks go to the members of the Laboratory for Genetics, University of Osnabrück, for their contributions, helpful advice and unflagging support. We gratefully acknowledge the linguistic revision by L. Schmieding. Publication of the results was funded by the ‘ZKfG’ of the University of Osnabrück.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E Peters.

Additional information

Becker and Nieberg have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Becker, L., Nieberg, C., Jahreis, K. et al. MHC class II variation in the endangered European mink Mustela lutreola (L. 1761)—consequences for species conservation. Immunogenetics 61, 281–288 (2009). https://doi.org/10.1007/s00251-009-0362-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-009-0362-2

Keywords

Navigation