Abstract
The MHC is one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. Apart from pathogen-mediated selection, sexual selection can also contribute to the maintenance of MHC diversity. MHC-dependent sexual selection could occur via several mechanisms but at present there is no consensus as to which of these mechanisms are involved and their importance. Previous studies have often suffered from limited genetic and behavioural data and small sample size, and were rarely able to examine all the mechanisms together, determine whether signatures of MHC-based non-random mating are independent of genomic effects or differentiate whether MHC-dependent sexual selection takes place at the pre- or post-copulatory stage. In this study, we use Monte Carlo simulation to investigate evidence for non-random MHC-dependent mating patterns by all three mechanisms in a free-living population of Soay sheep. Using 1710 sheep diplotyped at the MHC class IIa region and genome-wide SNPs, together with field observations of consorts, we found sexual selection against a particular haplotype in males at the pre-copulatory stage and sexual selection against female MHC heterozygosity during the rut. We also found MHC-dependent disassortative mating at the post-copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC-dependent disassortative mating could be a by-product of inbreeding avoidance. Our results therefore suggest that while multiple apparent mechanisms of non-random mating with respect to the MHC may occur, some of them have alternative explanations.
Highlights
Major histocompatibility complex (MHC) genes encode cell surface proteins that present pathogen-derived peptide to T cells to activate the adaptive immune response and are one of the most variable loci across the vertebrate genome
MHC-dependent sexual section could act through both intrasexual selection via male-male competition and through intersexual selection including mate choice based on the partner's MHC constitution or based on the MHC compatibility
We aimed to test for specific mechanisms of MHC-dependent sexual selection by asking the following questions: 1) Are individuals carrying specific MHC haplotypes favoured during mating? 2) Are MHC-heterozygote individuals favoured during mating? 3) Is there MHC-dependent disassortative or assortative mating? 4) If there is disassortative mating, is it based on haplotype divergence? 5) Is there inbreeding preference or avoidance? 6) If any signature of non-random mating is detected, does it occur at the pre-or post- copulatory stage? 7) If there is any signature of MHC-based mating, is this signature independent of genome-wide heterozygosity or relatedness?
Summary
Major histocompatibility complex (MHC) genes encode cell surface proteins that present pathogen-derived peptide to T cells to activate the adaptive immune response and are one of the most variable loci across the vertebrate genome. A recent study documented the impact of sample size on error rates and effect sizes and suggested a sample size of 500 mating pairs is required for testing MHC-dependent sexual selection (Hoover & Nevitt, 2016) which was not always available in previous studies. A previous study using five MHC-linked microsatellite loci genotyped in between 887 and 1209 individuals born between 1985 and 1994 found no evidence for MHC-dependent assortative or disassortative mating in this population (Paterson & Pemberton, 1997). This genetic and genomic data combined with a large number of consort and parentage records enabled us to test MHC-dependent sexual selection more thoroughly than before using Monte Carlo simulations. We aimed to test for specific mechanisms of MHC-dependent sexual selection by asking the following questions: 1) Are individuals carrying specific MHC haplotypes favoured during mating? We aimed to test for specific mechanisms of MHC-dependent sexual selection by asking the following questions: 1) Are individuals carrying specific MHC haplotypes favoured during mating? 2) Are MHC-heterozygote individuals favoured during mating? 3) Is there MHC-dependent disassortative or assortative mating? 4) If there is disassortative mating, is it based on haplotype divergence? 5) Is there inbreeding preference or avoidance? 6) If any signature of non-random mating is detected, does it occur at the pre-or post- copulatory stage? 7) If there is any signature of MHC-based mating, is this signature independent of genome-wide heterozygosity or relatedness?
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