Gene duplication and divergence produce divergent MHC genotypes without disassortative mating

Abstract Genes of the major histocompatibility complex ( MHC ) exhibit heterozygote advantage in immune defence, which in turn can select for MHC ‐disassortative mate choice. However, many species lack this expected pattern of MHC ‐disassortative mating. A possible explanation lies in evolutionary p...

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Bibliographic Details
Published in:Molecular Ecology
Main Authors: Dearborn, Donald C., Gager, Andrea B., McArthur, Andrew G., Gilmour, Morgan E., Mandzhukova, Elena, Mauck, Robert A.
Other Authors: Arthur Vining Davis Foundations, National Institute of General Medical Sciences, National Institutes of Health, Bates College, Cisco Systems Canada, Inc.
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2016
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Online Access:http://dx.doi.org/10.1111/mec.13747
https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fmec.13747
https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.13747
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Summary:Abstract Genes of the major histocompatibility complex ( MHC ) exhibit heterozygote advantage in immune defence, which in turn can select for MHC ‐disassortative mate choice. However, many species lack this expected pattern of MHC ‐disassortative mating. A possible explanation lies in evolutionary processes following gene duplication: if two duplicated MHC genes become functionally diverged from each other, offspring will inherit diverse multilocus genotypes even under random mating. We used locus‐specific primers for high‐throughput sequencing of two expressed MHC Class II B genes in Leach's storm‐petrels, Oceanodroma leucorhoa , and found that exon 2 alleles fall into two gene‐specific monophyletic clades. We tested for disassortative vs. random mating at these two functionally diverged Class II B genes, using multiple metrics and different subsets of exon 2 sequence data. With good statistical power, we consistently found random assortment of mates at MHC . Despite random mating, birds had MHC genotypes with functionally diverged alleles, averaging 13 amino acid differences in pairwise comparisons of exon 2 alleles within individuals. To test whether this high MHC diversity in individuals is driven by evolutionary divergence of the two duplicated genes, we built a phylogenetic permutation model. The model showed that genotypic diversity was strongly impacted by sequence divergence between the most common allele of each gene, with a smaller additional impact of monophyly of the two genes. Divergence of allele sequences between genes may have reduced the benefits of actively seeking MHC ‐dissimilar mates, in which case the evolutionary history of duplicated genes is shaping the adaptive landscape of sexual selection.