Is Mate Choice in Humans MHC-Dependent?

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Abstract
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−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. There has been a longstanding hypothesis that selection may have led to mating patterns that encourage heterozygosity at Major Histocompatibility Complex (MHC) loci because of improved immune response to pathogens in the offspring of such matings, and, indeed, this has been observed in several model systems. However, in humans, previous studies regarding the role of the MHC in mate choice or preference, both directly in couples and also indirectly in “sweaty T-shirts” experiments, have reported conflicting results. Here, by using genome-wide genotype data and HLA types in African and European American couples, we test whether humans tend to choose MHC-dissimilar mates. This approach allows us to distinguish MHC-specific effects from genome-wide effects. In the African sample, the patterns at MHC loci is confounded by genome-wide effects, possibly resulting from demographic processes relating to the social organization of this population, and no tendency to choose MHC-dissimilar mates is detected. On the other hand, the sampled European Americans appear to have favoured MHC-dissimilar mates, supporting the hypothesis that MHC influences mate choice in some human populations. Thus, this study suggests that, in some cases, humans may rely on biological factors, in addition to social factors, when choosing a mate.