Skip to main content
SpringerLink
Log in

Scent, Mate Choice and Genetic Heterozygosity

  • Conference paper
Chemical Signals in Vertebrates 11

Abstract

Females of many species choose to mate with relatively unrelated males in order to ensure outbred, heterozygous offspring. There is some evidence to suggest that the MHC is involved in mate choice decisions, either because MHC heterozygous offspring are more resistant to disease, or because the highly detectable odours associated with this region allow it to act as a marker of general inbreeding. To determine which role the MHC plays it is necessary to disentangle this region from the genetic background, a requirement which has generally proven difficult to achieve. We argue that the emphasis on MHC’s role in mate choice has resulted in other potential markers of inbreeding being neglected, and discuss the evidence for MHC disassortative mating, the interaction with genetic background, and a possible role for alternative markers of inbreeding.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aeschlimann, P.B., Häberli, M.A., Reusch, T.B.H., Boehm, T. and Milinski, M. (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav. Ecol. Sociobiol. 54, 119–126.

    Google Scholar 

  • Andrews, P.W. and Boyse, E.A. (1978) Mapping of an H-2-linked gene that influences mating preference in mice. Immunogenet. 6, 265–268.

    Article  Google Scholar 

  • Bernatchez, L. and Landry, C. (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J. Evol. Biol. 16, 363–377.

    Article  PubMed  CAS  Google Scholar 

  • Beynon, R.J. and Hurst, J.L. (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochemical Society Transactions 31, 142–146.

    Article  PubMed  CAS  Google Scholar 

  • Bixler, A. and Tang-Martinez, Z. (2006) Reproductive performance as a function of inbreeding in prairie voles (Microtus ochrogaster). J. Mammal. 87, 944–949.

    Article  Google Scholar 

  • Blouin, M.S., Parsons, M., Lacaille, V. and Lotz, S. (1996) Use of microsatellite loci to classify individuals by relatedness. Mol. Ecol. 5, 393–401.

    Article  PubMed  CAS  Google Scholar 

  • Brennan, P.A. and Kendrick, K.M. (2006) Mammalian social odours: attraction and individual recognition. Phil. Trans. R. Soc. B 361, 2061–2078.

    Article  PubMed  CAS  Google Scholar 

  • Brennan, P.A. and Zufall, F. (2006) Pheromonal communication in vertebrates. Nature 444, 308–315.

    Article  PubMed  CAS  Google Scholar 

  • Brown, J.L. (1997) A theory of mate choice based on heterozygosity. Behav. Ecol. 8, 60–65.

    Article  Google Scholar 

  • Brown, J.L. and Eklund, A.C. (1994) Kin recognition and the major histocompatibility complex: an integrative review. Am. Nat. 143, 435–461.

    Article  Google Scholar 

  • Byers, J.A. and Waits, L. (2006) Good genes sexual selection in nature. Proc. Natl. Acad. Sci. USA 103, 16343–16345.

    Article  PubMed  CAS  Google Scholar 

  • Carroll, L.S., Penn, D.J. and Potts, W.K. (2002) Discrimination of MHC-derived odors by untrained mice is consistent with divergence in peptide-binding region residues. Proc. Natl. Acad. Sci. USA 99, 2187–2192.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth, D. and Charlesworth, B. (1987) Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18, 237–268.

    Article  Google Scholar 

  • Cheetham, S.A., Thom, M.D., Jury, F., Ollier, W.E.R., Beynon, R.J. and Hurst, J.L. (2007) MUPs not MHC provide a specific signal for individual recognition in wild house mice. Unpublished manuscript.

    Google Scholar 

  • Coltman, D.W., Bowen, W.D. and Wright, J.M. (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. B 265, 803–809.

    Article  PubMed  CAS  Google Scholar 

  • Coltman, D.W., Pilkington, J.G., Smith, J.A. and Pemberton, J.M. (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53, 1259–1267.

    Article  Google Scholar 

  • Cooney, R. and Bennett, N.C. (2000) Inbreeding avoidance and reproductive skew in a cooperative mammal. Proc. R. Soc. B 267, 801–806.

    Article  PubMed  CAS  Google Scholar 

  • Crnokrak, P. and Roff, D.A. (1999) Inbreeding depression in the wild. Heredity 83, 260–270.

    Article  PubMed  Google Scholar 

  • Doherty, P.C. and Zinkernagel, R.M. (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 complex. Nature 256, 50–52.

    Article  PubMed  CAS  Google Scholar 

  • Drickamer, L.C., Gowaty, P.A. and Holmes, C.M. (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim. Behav. 59, 371–378.

    Article  PubMed  Google Scholar 

  • Egid, K. and Brown, J.L. (1989) The major histocompatibility complex and female mating preferences in mice. Anim. Behav. 38, 548–550.

    Article  Google Scholar 

  • Hughes, A.L. and Nei, M. (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170.

    Article  PubMed  CAS  Google Scholar 

  • Humphries, R.E., Robertson, D.H.L., Beynon, R.J. and Hurst, J.L. (1999) Unravelling the chemical basis of competitive scent marking in house mice. Anim. Behav. 58, 1177–1190.

    Article  PubMed  Google Scholar 

  • Hurst, J.L., Payne, C.E., Nevison, C.M., Marie, A.D., Humphries, R.E., Robertson, D.H.L., Cavaggioni, A. and Beynon, R.J. (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414, 631–634.

    Article  PubMed  CAS  Google Scholar 

  • Hurst, J.L., Thom, M.D., Nevison, C.M., Humphries, R.E. and Beynon, R.J. (2005) MHC odours are not required or sufficient for recognition of individual scent owners. Proc. R. Soc. B 272, 715–724.

    Article  PubMed  Google Scholar 

  • Jiménez, J.A., Hughes, K.A., Alaks, G., Graham, L. and Lacy, R.C. (1994) An experimental study of inbreeding depression in a natural habitat. Science 266, 271–273.

    Article  PubMed  Google Scholar 

  • Jordan, W.C. and Bruford, M.W. (1998) New perspectives on mate choice and the MHC. Heredity 81, 239–245.

    Article  PubMed  CAS  Google Scholar 

  • Keane, B., Creel, S.R. and Waser, P.M. (1996) No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behav. Ecol. 7, 480–489.

    Article  CAS  Google Scholar 

  • Keller, L.F. (1998) Inbreeding and its fitness effects in an insular population of sparrows (Melospiza melodia). Evolution 52, 240–250.

    Article  Google Scholar 

  • Keller, L.F., Arcese, P., Smith, J.N.M., Hochachka, W.M. and Stearns, S.C. (1994) Selection against inbred song sparrows during a natural population bottleneck. Nature 372, 356–357.

    Article  PubMed  CAS  Google Scholar 

  • Keller, L.F. and Waller, D.M. (2002) Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241.

    Article  Google Scholar 

  • Koenig, W.D., Stanback, M.T. and Haydock, J. (1999) Demographic consequences of incest avoidance in the cooperatively breeding acorn woodpecker. Anim. Behav. 57, 1287–1293.

    Article  PubMed  Google Scholar 

  • Krackow, S. and Matuschak, B. (1991) Mate choice for non-siblings in wild mice - evidence from a choice test and a reproductive test. Ethology 88, 99–108.

    Article  Google Scholar 

  • Kurtz, J., Kalbe, M., Aeschlimann, P.B., Häberli, M.A., Wegner, K.M., Reusch, T.B.H. and Milinski, M. (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc. R. Soc. B 271, 197–204.

    Article  PubMed  CAS  Google Scholar 

  • Landry, C., Garant, D., Duchesne, P. and Bernatchez, L. (2001) ’Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. B 268, 1279–1285.

    Article  PubMed  CAS  Google Scholar 

  • Langefors, A., Lohm, J., Grahn, M., Andersen, O. and von Schantz, T. (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc. R. Soc. B 268, 479–485.

    Article  PubMed  CAS  Google Scholar 

  • Leinders-Zufall, T., Brennan, P., Widmayer, P., Chandramani, P., Maul-Pavicic, A., Jager, M., Li, X.H., Breer, H., Zufall, F. and Boehm, T. (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033–1037.

    Article  PubMed  CAS  Google Scholar 

  • Mays, H.L. and Hill, G.E. (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol. Evol. 19, 554–559.

    Article  PubMed  Google Scholar 

  • Meagher, S., Penn, D.J. and Potts, W.K. (2000) Male-male competition magnifies inbreeding depression in wild house mice. Proc. Natl. Acad. Sci. USA 97, 3324–3329.

    Article  PubMed  CAS  Google Scholar 

  • Milinski, M. (2006) The major histocompatibility complex, sexual selection, and mate choice. Ann. Rev. Ecol. Evol. Sys. 2006, 159–186.

    Article  Google Scholar 

  • O’Riain, M.J., Bennett, N.C., Brotherton, P.N.M., McIlrath, G. and Clutton-Brock, T.H. (2000) Reproductive supression and inbreeding avoidance in wild populations of co-operatively breeding meerkats (Suricata suricatta). Behav. Ecol. Sociobiol. 48, 471–477.

    Article  Google Scholar 

  • Olsén, K.H., Grahn, M., Lohm, J. and Langefors, Å. (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim. Behav. 56, 319–327.

    Article  PubMed  Google Scholar 

  • Olsson, M., Madsen, T., Nordby, J., Wapstra, E., Ujvari, B. and Wittsell, H. (2003) Major histocompatibility complex and mate choice in sand lizards. Proc. R. Soc. B 270, S254–S256.

    Article  PubMed  CAS  Google Scholar 

  • Parrott, M.L., Ward, S.J. and Temple-Smith, P.D. (2007) Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis). Behav. Ecol. Sociobiol., DOI:10.1007/s00265-006-0340-8.

    Google Scholar 

  • Paterson, S., Wilson, K. and Pemberton, J.M. (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aires L.). Proc. Natl. Acad. Sci. USA 95, 3714–3719.

    Article  PubMed  CAS  Google Scholar 

  • Penn, D.J. (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108, 1–21.

    Article  Google Scholar 

  • Penn, D.J., Damjanovich, K. and Potts, W.K. (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc. Natl. Acad. Sci. USA 99, 11260–11264.

    Article  PubMed  CAS  Google Scholar 

  • Persaud, K.N. and Galef, B.G. (2005) Eggs of a female Japanese quail are more likely to be fertilized by a male that she prefers. J. Comp. Psych. 119, 251–256.

    Article  Google Scholar 

  • Potts, W.K., Manning, C.J. and Wakeland, E.K. (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352, 619–621.

    Article  PubMed  CAS  Google Scholar 

  • Potts, W.K., Manning, C.J. and Wakeland, E.K. (1994) The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test. Phil. Trans. R. Soc. B 346, 369–378.

    Article  PubMed  CAS  Google Scholar 

  • Pusey, A. and Wolf, M. (1996) Inbreeding avoidance in mammals. Trends Ecol. Evol. 11, 201–206.

    Article  Google Scholar 

  • Pusey, A.E. (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol. Evol. 2, 295–299.

    Article  Google Scholar 

  • Ralls, K., Ballou, J.D. and Templeton, A. (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol. 2, 185–193.

    Article  Google Scholar 

  • Rauch, R., Kalbe, M. and Reusch, T.B.H. (2006) Relative importance of MHC and genetic background for parasite load in a field experiment. Evol. Ecol. Res. 8, 373–386.

    Google Scholar 

  • Reusch, T.B.H., Häberli, M.A., Aeschlimann, P.B. and Milinski, M. (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414, 300–302.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, D.H.L., Cox, K.A., Gaskell, S.J., Evershed, R.P. and Beynon, R.J. (1996) Molecular heterogeneity in the major urinary proteins of the house mouse Mus musculus. Biochem. J. 316, 265–272.

    PubMed  CAS  Google Scholar 

  • Ryan, K.K. and Lacy, R.C. (2003) Monogamous male mice bias behaviour towards females according to very small differences in kinship. Anim. Behav. 65, 379–384.

    Article  Google Scholar 

  • Sato, A., Figueroa, F., Murray, B.W., Malaga-Trillo, E., Zaleska-Rutczynska, Z., Sultmann, H., Toyosawa, S., Wedekind, C., Steck, N. and Klein, J. (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenet. 51, 108–116.

    Article  CAS  Google Scholar 

  • Schellinck, H.M., Slotnick, B.M. and Brown, R.E. (1997) Odors of individuality originating from the major histocompatibility complex are masked by diet cues in the urine of rats. Anim. Learn. Behav. 25, 193–199.

    Google Scholar 

  • Seddon, N., Amos, W., Mulder, R.A. and Tobias, J.A. (2004) Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird. Proc. R. Soc. B 271, 1823–1829.

    Article  PubMed  Google Scholar 

  • Sherborne, A.L., Thom, M.D., Paterson, S., Jury, F., Ollier, W.E.R., Stockley, P., Beynon, R.J. and Hurst, J.L. (2007) The molecular basis of inbreeding avoidance in house mice. Submitted.

    Google Scholar 

  • Simmons, L.W. (1991) Female choice and relatedness of mates in the field cricket, Gryllus bimaculatus. Anim. Behav. 41, 493–501.

    Article  Google Scholar 

  • Slate, J., Kruuk, L.E.B., Marshall, T.C., Pemberton, J.M. and Clutton-Brock, T.H. (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc. R. Soc. B 267, 1657–1662.

    Article  PubMed  CAS  Google Scholar 

  • Slate, J. and Pemberton, J.M. (2002) Comparing molecular measures for detecting inbreeding depression. J. Evol. Biol. 15, 20–31.

    Article  Google Scholar 

  • Smith, D.G. (1995) Avoidance of close consanguineous inbreeding in captive groups of rhesus macaques. Am. J. Primatol. 35, 31–40.

    Article  Google Scholar 

  • Soltis, J., Mitsunaga, F., Shimizu, K., Yanagihara, Y. and Nozaki, M. (1999) Female mating strategy in an enclosed group of Japanes macaques. Am. J. Primatol. 47, 263–278.

    Article  PubMed  CAS  Google Scholar 

  • Spehr, M., Kelliher, K.R., Li, X.H., Boehm, T., Leinders-Zufall, T. and Zufall, F. (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 26, 1961–1970.

    Article  PubMed  CAS  Google Scholar 

  • Stockley, P., Searle, J.B., Macdonald, D.W. and Jones, C.S. (1993) Female multiple mating-behaviour in the common shrew as a strategy to reduce inbreeding. Proc. R. Soc. B 254, 173–179.

    Article  PubMed  CAS  Google Scholar 

  • Thornhill, R., Gangestad, S.W., Miller, R., Scheyd, G., McCullough, J.K. and Franklin, M. (2003) Major histocompatibility genes, symmetry and body scent attractiveness in men and women. Behav. Ecol. 14, 668–678.

    Article  Google Scholar 

  • Tregenza, T. and Wedell, N. (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013–1027.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wedekind, C., Walker, M. and Little, T.J. (2005) The course of malaria in mice: major histocompatibility complex (MHC) effects, but no general MHC heterozygosity advantage in single-strain infections. Genetics 170, 1427–1430.

    Article  PubMed  CAS  Google Scholar 

  • Wedekind, C., Walker, M. and Little, T.J. (2006) The separate and combined effects of MHC genotype, parasite clone, and host gender on the course of malaria in mice. BMC Genetics 7, 55.

    Article  PubMed  CAS  Google Scholar 

  • Wegner, K.M., Kalbe, M., Kurtz, J., Reusch, T.B.H. and Milinski, M. (2003) Parasite selection for immunogenetic optimality. Science 301, 1343.

    Article  PubMed  CAS  Google Scholar 

  • Westerdahl, H., Waldenström, J., Hansson, B., Hasselquist, D., Von Schantz, T. and Bensch, S. (2005) Associations between malaira and MHC genes in a migratory songbird. Proc. R. Soc. B 272, 1511–1518.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi, M., Yamazaki, K., Beauchamp, G.K., Bard, J., Thomas, L. and Boyse, E.A. (1981) Distinctive urinary odors governed by the major histocompatibility locus of the mouse. Proc. Natl. Acad. Sci. USA 78, 5817–5820.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, K., Beauchamp, G.K., Bard, J., Thomas, L. and Boyse, E.A. (1982) Chemosensory recognition of phenotypes determined by the Tla and H-2K regions of chromosome 17 of the mouse. Proc. Natl. Acad. Sci. USA 79, 7828–7831.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, K., Beauchamp, G.K., Egorov, I.K., Bard, J., Thomas, L. and Boyse, E.A. (1983) Sensory distinction between H-2b and H-2bm1 mutant mice. Proc. Natl. Acad. Sci. USA 80, 5685–5688.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, K., Boyse, E.A., Miké, V., Thaler, H.T., Mathieson, B.J., Abbott, J., Boyse, J., Zayas, Z.A. and Thomas, L. (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J. Exp. Med. 144, 1324–1335.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, K., Yamaguchi, M., Andrews, P.W., Peake, B. and Boyse, E.A. (1978) Mating preferences of F2 segregants of crosses between MHC-congenic mouse strains. Immunogenet. 6, 253–259.

    Article  Google Scholar 

  • Zeh, J.A. and Zeh, D.W. (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc. R. Soc. B 263, 1711–1717.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Veterinary Preclinical Science, University of Liverpool, Leahurst, Neston CH64 7TE, UK

    Michael D. Thom

Authors
  1. Michael D. Thom
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Stockley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert J. Beynon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jane L. Hurst
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Veterinary Preclinical Science, University of Liverpool, Leahurst, Neston CH64 7TE, UK

    Jane L. Hurst

  2. Department of Veterinary Preclinical Science, University of Liverpool, Crown Street, Liverpool, L69 7ZJ, UK

    Robert J. Beynon

  3. School of Biological Sciences, University of Liverpool, Crown Street, Liverpool, L69 7ZB, UK

    S. Craig Roberts

  4. Office of Distance and Online Learning, University of Oxford, Oxford OX2 7DD, UK

    Tristram D. Wyatt

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media,LLC

About this paper

Cite this paper

Thom, M.D., Stockley, P., Beynon, R.J., Hurst, J.L. (2008). Scent, Mate Choice and Genetic Heterozygosity. In: Hurst, J.L., Beynon, R.J., Roberts, S.C., Wyatt, T.D. (eds) Chemical Signals in Vertebrates 11. Springer, New York, NY. https://doi.org/10.1007/978-0-387-73945-8_28

Download citation

Publish with us

Policies and ethics

Search

Navigation