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Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism

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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Figure 1: Frequency distribution of the number of MHC class-IIB alleles (peptide-binding region) detectable by SSCP in 144 fish from one population (Schöhsee).
Figure 2: Odour preference of gravid female three-spined stickleback for males in a flow tank.

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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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Correspondence to Thorsten B. H. Reusch.

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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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