Is mate choice in humans MHC-Dependent?

Department of Statistics, University of Oxford, Oxford, United Kingdom.
PLoS Genetics (Impact Factor: 7.53). 10/2008; 4(9):e1000184. DOI: 10.1371/journal.pgen.1000184
Source: PubMed


In several species, including rodents and fish, it has been shown that the Major Histocompatibility Complex (MHC) influences mating preferences and, in some cases, that this may be mediated by preferences based on body odour. In humans, the picture has been less clear. Several studies have reported a tendency for humans to prefer MHC-dissimilar mates, a sexual selection that would favour the production of MHC-heterozygous offspring, who would be more resistant to pathogens, but these results are unsupported by other studies. Here, we report analyses of genome-wide genotype data (from the HapMap II dataset) and HLA types in African and European American couples to test whether humans tend to choose MHC-dissimilar mates. In order to distinguish MHC-specific effects from genome-wide effects, the pattern of similarity in the MHC region is compared to the pattern in the rest of the genome. African spouses show no significant pattern of similarity/dissimilarity across the MHC region (relatedness coefficient, R = 0.015, p = 0.23), whereas across the genome, they are more similar than random pairs of individuals (genome-wide R = 0.00185, p<10(-3)). We discuss several explanations for these observations, including demographic effects. On the other hand, the sampled European American couples are significantly more MHC-dissimilar than random pairs of individuals (R = -0.043, p = 0.015), and this pattern of dissimilarity is extreme when compared to the rest of the genome, both globally (genome-wide R = -0.00016, p = 0.739) and when broken into windows having the same length and recombination rate as the MHC (only nine genomic regions exhibit a higher level of genetic dissimilarity between spouses than does the MHC). This study thus supports the hypothesis that the MHC influences mate choice in some human populations.

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    • "There is increasing support for the suggestion that MHC constitution is olfactorily perceptible in a variety of taxa (Leinders-Zufall et al., 2004; Milinski et al., 2005; Radwan et al., 2008); hence, individual odour profiles are often predicted to be the cues for MHC dissimilarity. Major histocompatibility complex-based disassortative mating preferences have been reported across taxa, both in model species (Potts et al., 1991; Ober et al., 1997; Chaix et al., 2008) and in wild populations of nonmodel species (Consuegra & Garcia de Leaniz, 2008; Juola & Dearborn, 2011; – but see Huchard et al., 2010a). Although a number of studies suggested that females target MHC per se, by mating with MHC dissimilar (Landry et al., 2001; Miller et al., 2009) or optimally dissimilar males (Forsberg et al., 2007; Eizaguirre et al., 2009), other studies could not differentiate the role of inbreeding avoidance or MHC diversity on mate choice decisions (Freeman-Gallant et al., 2003; Setchell et al., 2010). "
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    ABSTRACT: Genes of the major histocompatibility complex (MHC) are regarded as a potentially important target of mate choice due to the fitness benefits that may be conferred to the offspring. According to the complementary genes hypothesis, females mate with MHC dissimilar males to enhance the immunocompetence of their offspring or to avoid inbreeding depression. Here, we investigate whether selection favours a preference for maximally dissimilar or optimally dissimilar MHC class I types, based on MHC genotypes, average amino acid distances and the functional properties of the antigen-binding sites (MHC supertypes); and whether MHC type dissimilarity predicts relatedness between mates in a wild great tit population. In particular, we explore the role that MHC class I plays in female mate choice decisions while controlling for relatedness and spatial population structure, and examine the reproductive fitness consequences of MHC compatibility between mates. We find no evidence for the hypotheses that females select mates on the basis of either maximal or optimal MHC class I dissimilarity. A weak correlation between MHC allele sharing and relatedness, and between MHC supertype sharing and relatedness suggests that MHC dissimilarity at functional variants may not provide an effective index of relatedness. Moreover the reproductive success of pairs did not vary with MHC dissimilarity. Our results provide no support for the suggestion that selection favours, or that mate choice realises, a preference for complimentary MHC types. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Full-text · Article · Feb 2015 · Journal of Evolutionary Biology
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    • "The null results of previous studies might simply be attributed to lack of power due to small sample sizes in attempting to determine a complex human behavior with multiple intervening variables. Most recently Chaix et al. (2008) showed that MHC mate selection is apparent in European and American populations, but not in African Yoruba populations. However, the statistical methods of testing their hypothesis was criticized, because the significance could be attribute to extreme mate pairs within the groups, as well as for not correctly adjusting their statistical thresholds for multiple hypothesis testing (Derti et al., 2010). "
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    • "Beyond transplantation, polymorphisms in the MHC region have been used as molecular markers for population genetics and studies of diseases and traits. In the past 30 years, no other region in the genome has provided more association signals with multifactorial traits, including autoimmune diseases [5]–[8], inflammatory and infectious diseases [9], cancer [10], adverse drug effects [11], [12], and behavioral traits such as mating [13], [14]. To assess HLA allelic diversity, these studies employed a broad range of methodologies from serology, restriction fragment length polymorphism, and microsatellites up to the latest generation of single nucleotide polymorphism (SNP) genotyping methods. "
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    ABSTRACT: The 1000 Genomes Project aims to provide a deep characterization of human genome sequence variation by sequencing at a level that should allow the genome-wide detection of most variants with frequencies as low as 1%. However, in the major histocompatibility complex (MHC), only the top 10 most frequent haplotypes are in the 1% frequency range whereas thousands of haplotypes are present at lower frequencies. Given the limitation of both the coverage and the read length of the sequences generated by the 1000 Genomes Project, the highly variable positions that define HLA alleles may be difficult to identify. We used classical Sanger sequencing techniques to type the HLA-A, HLA-B, HLA-C, HLA-DRB1 and HLA-DQB1 genes in the available 1000 Genomes samples and combined the results with the 103,310 variants in the MHC region genotyped by the 1000 Genomes Project. Using pairwise identity-by-descent distances between individuals and principal component analysis, we established the relationship between ancestry and genetic diversity in the MHC region. As expected, both the MHC variants and the HLA phenotype can identify the major ancestry lineage, informed mainly by the most frequent HLA haplotypes. To some extent, regions of the genome with similar genetic or similar recombination rate have similar properties. An MHC-centric analysis underlines departures between the ancestral background of the MHC and the genome-wide picture. Our analysis of linkage disequilibrium (LD) decay in these samples suggests that overestimation of pairwise LD occurs due to a limited sampling of the MHC diversity. This collection of HLA-specific MHC variants, available on the dbMHC portal, is a valuable resource for future analyses of the role of MHC in population and disease studies.
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