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Balancing selection, sexual selection and geographic structure in MHC genes of Great Snipe

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Abstract

Signatures of balancing selection are often found when investigating the extremely polymorphic regions of major histocompatibility complex (MHC) genes, and it is generally accepted that selective forces maintain this polymorphism. However, the exact nature of the selection is controversial. Theoretical studies have mainly focused on overdominance and/or frequency dependent selection while laboratory studies have emphasised the role of mate choice. Empirical field data, on the other hand, have been relatively scarce. Previously we have found that geographic structure in MHC class II genes of the Great Snipe (Gallinago media) is too pronounced to be explained by neutral forces alone. Here we test the hypothesis that sexual selection on MHC alleles may be influencing this geographic structure between mountain and lowland populations. We found evidence of balancing selection acting on MHC genes in the form of a higher rate of amino-acid changing substitutions compared to silent substitutions in the peptide binding regions. Not only natural selection but also sexual selection may influence MHC polymorphism in this bird because certain MHC alleles have been found to be associated with higher male mating success. Contrary to predictions from negative frequency dependent selection, males carrying locally rare alleles did not have a mating advantage. Instead, the mating success of alleles in a mountain population was positively correlated to their relative frequency in the mountains compared to the lowlands, implying that locally adapted MHC alleles may also be favoured by sexual selection.

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Acknowledgments

We thank all assistants and students for help with field- and lab work. Many thanks to the participants of the ecological genomics workshop 2007 for interesting discussions and valuable feedback on the issues presented here. Thanks also to D. Alongi Johnson, J. Stapley and two anonymous referees for commenting on previous versions of this manuscript. Permissions for ringing and blood sampling were given from the Stavanger Museum, Swedish Bird Ringing Centre, Norwegian Animal Research Authority and Uppsala Djurförsöksetiska Nämnd. Bjurzons, Liljewalchs resistipendium, Royal Swedish Academy of Sciences and the Research Council of Norway provided financial support for this study.

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Correspondence to Robert Ekblom.

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Ekblom, R., Sæther, S.A., Fiske, P. et al. Balancing selection, sexual selection and geographic structure in MHC genes of Great Snipe. Genetica 138, 453–461 (2010). https://doi.org/10.1007/s10709-008-9335-x

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  • DOI: https://doi.org/10.1007/s10709-008-9335-x

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