Female-mediated selective sperm activation may remodel major histocompatibility complex-based mate choice decisions in humans

Major histocompatibility complex (MHC) genes are known to mediate mate choice both at the individual and gamete level. However, it has remained unclear how different episodes of MHC-associated mate choice interact and contribute to the total selection on MHC genes. Here, we clarified this interaction in humans by performing a full-factorial experiment where 10 females first ranked the attractiveness and intensity of the body odours of 11 males. Then we studied whether female odour preferences in these same 110 male-female combinations predicted sperm performance in the presence of follicular fluid (sperm-stimulating female reproductive fluid). When analyzing the total MHC similarity (including classical and non-classical MHC genes) of the male-female combinations, we found that females preferred the body odours of MHC-similar males, but that sperm motility was positively affected by the MHC dissimilarity of the male-female combinations. No associations were found for classical MHC genes only. Furthermore, odour preferences were negatively associated with sperm motility at the end of the follicular fluid treatment. Together, our results indicate that individual and gamete-level mate choice processes may act in opposing directions and that the most attractive males are not necessarily the most optimal partners at the post-copulatory level. Finally, our findings suggest that gamete-mediated mate choice may have a definitive role in disfavouring genetically incompatible partners from fertilizing oocytes.