Abstract
The origin and maintenance of polymorphism in major histocompatibility complex (MHC) genes in natural populations is still unresolved1. Sexual selection, frequency-dependent selection by parasites and pathogens, and heterozygote advantage have been suggested to explain the maintenance of high allele diversity at MHC genes2,3,4. Here we argue that there are two (non-exclusive) strategies for MHC-related sexual selection, representing solutions to two different problems: inbreeding avoidance and parasite resistance. In species prone to inadvertent inbreeding, partners should prefer dissimilar MHC genotypes to similar ones. But if the goal is to maximize the resistance of offspring towards potential infections, the choosing sex should prefer mates with a higher diversity of MHC alleles. This latter strategy should apply when there are several MHC loci, as is the case in most vertebrates2,5. We tested the relative importance of an ‘allele counting’ strategy compared to a disassortative mating strategy using wild-caught three-spined sticklebacks (Gasterosteus aculeatus) from an interconnected system of lakes. Here we show that gravid female fish preferred the odour of males with a large number of MHC class-IIB alleles to that of males with fewer alleles. Females did not prefer male genotypes dissimilar to their own.
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References
Apanius, V., Penn, D., Slev, P. R., Ruff, L. R. & Potts, W. K. The nature of selection on the major histocompatibility complex. Crit. Rev. Immunol. 17, 179–224 (1997).
Klein, J. Natural History of the Major Histocompatibility Complex 615–620 (Wiley, New York, 1986).
Penn, D. & Potts, W. K. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153, 145–164 (1999).
Edwards, S. V. & Hedrick, P. W. Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol. Evol. 13, 305–311 (1998).
Kasahara, M. The chromosomal duplication model of the major histocompatibility complex. Crit. Rev. Immunol. 167, 17–32 (1999).
Darwin, C. The Origin of Species by Means of Natural Selection 88 (Murray, London, 1859).
Hamilton, W. D. & Zuk, M. Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387 (1982).
Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, New Jersey, 1994).
Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites. Proc. Natl Acad. Sci. USA 87, 3566–3573 (1990).
Brown, J. L. A theory of mate choice based on heterozygosity. Behav. Ecol. 8, 60–65 (1997).
Potts, W. K., Manning, C. J. & Wakeland, E. K. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352, 619–621 (1991).
Ober, C. et al. HLA and mate choice in humans. Am. J. Hum. Genet. 61, 497–504 (1997).
Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. MHC-dependent mate preferences in humans. Proc. R. Soc. Lond. B 260, 245–249 (1995).
Potts, W. K. & Slev, P. R. Pathogen-based models favoring MHC-genetic diversity. Immunol. Rev. 143, 181–197 (1995).
Sato, A., Figueroa, F., O'Huigin, C., Steck, N. & Klein, J. Cloning of major histocompatibility complex (MHC)-genes from threespine stickleback, Gasterosteus aculeatus. Mol. Mar. Biol. Biotechnol. 7, 221–231 (1998).
Yamazaki, K. et al. Control of mating preferences in mice by genes in the major histocompatibility complex. J. Exp. Med. 144, 1324–1335 (1976).
Brown, R. E., Roser, B. & Singh, P. B. Class I and class II regions of the major histocompatibility complex both contribute to individual odors in congenic inbred strains of rats. Behav. Genet. 19, 659–674 (1989).
Singh, P. B., Brown, R. E. & Roser, B. MHC antigens in urine as olfactory recognition cues. Nature 327, 161–164 (1987).
Penn, D. & Potts, W. K. How do major histocompatibility complex genes influence odor and mating preferences? Adv. Immunol. 69, 411–435 (1998).
Nowak, M. A., Tarczy-Hornoch, K. & Austyn, J. M. The optimal number of major histocompatibility complex molecules in an individual. Proc. Natl Acad. Sci. USA 89, 10896–10899 (1992).
Wootton, R. J. in The Biology of Sticklebacks (ed. Wootton, R. J.) 75–98 (Academic, New York, 1976).
Steck, N., Wedekind, C. & Milinski, M. No sibling odor preference in juvenile three-spined sticklebacks. Behav. Ecol. 10, 493–497 (1999).
Yamazaki, K. et al. Familial imprinting determines H-2 selective mating preferences. Science 240, 1331–1332 (1988).
Landry, C., Garant, D., Duchesne, P. & Bernatchez, L. Good genes as heterozygosity: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. Lond. B 268, 1279–1285 (2001).
Binz, T., Reusch, T. B. H., Wedekind, C. & Milinski, M. SSCP analysis of Mhc class II B genes in the threespine stickleback. J. Fish Biol. 58, 887–890 (2001).
Largiadèr, C. R., Fries, V., Kobler, B. & Bakker, C. M. Isolation and characterization of microsatellite loci from the three-spine stickleback, Gasterosteus aculeatus. Mol. Ecol. 8, 342–344 (1999).
Coulson, T. N. et al. Microsatellites measure inbreeding depression and heterosis in red deer. Proc. R. Soc. Lond. B 265, 489–495 (1998).
Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).
Acknowledgements
J. Kurtz, Å. Langefors, D. Penn and W. K. Potts improved earlier versions of the manuscript. We thank S. Liedtke for laboratory assistance, H. Deiwick and D. Lemcke for technical support, and G. Augustin for maintaining the aquaria. P.A. and M.H. were supported by the Swiss National Fund.
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Reusch, T., Häberli, M., Aeschlimann, P. et al. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414, 300–302 (2001). https://doi.org/10.1038/35104547
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DOI: https://doi.org/10.1038/35104547
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