Scent, Mate Choice and Genetic Heterozygosity

  • Michael D. Thom
  • Paula Stockley
  • Robert J. Beynon
  • Jane L. Hurst

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.

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References

  1. 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
  2. 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.CrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Bixler, A. and Tang-Martinez, Z. (2006) Reproductive performance as a function of inbreeding in prairie voles (Microtus ochrogaster). J. Mammal. 87, 944–949.CrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. Brennan, P.A. and Kendrick, K.M. (2006) Mammalian social odours: attraction and individual recognition. Phil. Trans. R. Soc. B 361, 2061–2078.PubMedCrossRefGoogle Scholar
  8. Brennan, P.A. and Zufall, F. (2006) Pheromonal communication in vertebrates. Nature 444, 308–315.PubMedCrossRefGoogle Scholar
  9. Brown, J.L. (1997) A theory of mate choice based on heterozygosity. Behav. Ecol. 8, 60–65.CrossRefGoogle Scholar
  10. Brown, J.L. and Eklund, A.C. (1994) Kin recognition and the major histocompatibility complex: an integrative review. Am. Nat. 143, 435–461.CrossRefGoogle Scholar
  11. Byers, J.A. and Waits, L. (2006) Good genes sexual selection in nature. Proc. Natl. Acad. Sci. USA 103, 16343–16345.PubMedCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. Charlesworth, D. and Charlesworth, B. (1987) Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18, 237–268.CrossRefGoogle Scholar
  14. 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
  15. 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.PubMedCrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. Cooney, R. and Bennett, N.C. (2000) Inbreeding avoidance and reproductive skew in a cooperative mammal. Proc. R. Soc. B 267, 801–806.PubMedCrossRefGoogle Scholar
  18. Crnokrak, P. and Roff, D.A. (1999) Inbreeding depression in the wild. Heredity 83, 260–270.PubMedCrossRefGoogle Scholar
  19. Doherty, P.C. and Zinkernagel, R.M. (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 complex. Nature 256, 50–52.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. Egid, K. and Brown, J.L. (1989) The major histocompatibility complex and female mating preferences in mice. Anim. Behav. 38, 548–550.CrossRefGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. Jordan, W.C. and Bruford, M.W. (1998) New perspectives on mate choice and the MHC. Heredity 81, 239–245.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Keller, L.F. (1998) Inbreeding and its fitness effects in an insular population of sparrows (Melospiza melodia). Evolution 52, 240–250.CrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. Keller, L.F. and Waller, D.M. (2002) Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241.CrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedCrossRefGoogle Scholar
  40. Milinski, M. (2006) The major histocompatibility complex, sexual selection, and mate choice. Ann. Rev. Ecol. Evol. Sys. 2006, 159–186.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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
  45. 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.PubMedCrossRefGoogle Scholar
  46. Penn, D.J. (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108, 1–21.CrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. Pusey, A. and Wolf, M. (1996) Inbreeding avoidance in mammals. Trends Ecol. Evol. 11, 201–206.CrossRefGoogle Scholar
  52. Pusey, A.E. (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol. Evol. 2, 295–299.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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
  55. 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.PubMedCrossRefGoogle Scholar
  56. 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.PubMedGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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
  62. Simmons, L.W. (1991) Female choice and relatedness of mates in the field cricket, Gryllus bimaculatus. Anim. Behav. 41, 493–501.CrossRefGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. Slate, J. and Pemberton, J.M. (2002) Comparing molecular measures for detecting inbreeding depression. J. Evol. Biol. 15, 20–31.CrossRefGoogle Scholar
  65. Smith, D.G. (1995) Avoidance of close consanguineous inbreeding in captive groups of rhesus macaques. Am. J. Primatol. 35, 31–40.CrossRefGoogle Scholar
  66. 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.PubMedCrossRefGoogle Scholar
  67. 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.PubMedCrossRefGoogle Scholar
  68. 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.PubMedCrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. Tregenza, T. and Wedell, N. (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013–1027.PubMedCrossRefGoogle Scholar
  71. Wedekind, C., Seebeck, T., Bettens, F. and Paepke, A. (1995) MHC-dependent mate preferences in humans. Proc. R. Soc. B 260, 245–249.PubMedCrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.PubMedCrossRefGoogle Scholar
  74. Wegner, K.M., Kalbe, M., Kurtz, J., Reusch, T.B.H. and Milinski, M. (2003) Parasite selection for immunogenetic optimality. Science 301, 1343.PubMedCrossRefGoogle Scholar
  75. 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.PubMedCrossRefGoogle Scholar
  76. 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.PubMedCrossRefGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar
  78. 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.PubMedCrossRefGoogle Scholar
  79. 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.PubMedCrossRefGoogle Scholar
  80. 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.CrossRefGoogle Scholar
  81. 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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media,LLC 2008

Authors and Affiliations

  • Michael D. Thom
    • 1
  • Paula Stockley
  • Robert J. Beynon
  • Jane L. Hurst
  1. 1.Department of Veterinary Preclinical ScienceUniversity of LiverpoolLeahurstUK

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