Cryptic female choice favours sperm from major histocompatibility complex-dissimilar males

Abstract

Cryptic female choice may enable polyandrous females to avoid inbreeding or bias offspring variability at key loci after mating. However, the role of these genetic benefits in cryptic female choice remains poorly understood. Female red junglefowl, Gallus gallus, bias sperm use in favour of unrelated males. Here, we experimentally investigate whether this bias is driven by relatedness per se, or by similarity at the major histocompatibility complex (MHC), genes central to vertebrate acquired immunity, where polymorphism is critical to an individual's ability to combat pathogens. Through experimentally controlled natural matings, we confirm that selection against related males' sperm occurs within the female reproductive tract but demonstrate that this is more accurately predicted by MHC similarity: controlling for relatedness per se, more sperm reached the eggs when partners were MHC-dissimilar. Importantly, this effect appeared largely owing to similarity at a single MHC locus (class I minor). Further, the effect of MHC similarity was lost following artificial insemination, suggesting that male phenotypic cues might be required for females to select sperm differentially. These results indicate that postmating mechanisms that reduce inbreeding may do so as a consequence of more specific strategies of cryptic female choice promoting MHC diversity in offspring.

Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha)

“…Thus, the observed mate compatibility, which explains roughly 44% of the variation in sperm velocity (42-45% across models), appears to be characterized by factors other than MHC, potentially by other peptides identified in the ovarian fluid of Chinook salmon (Johnson et al, 2014). MHC-dependent fertilization success was reported in mice (Wedekind et al, 1996;Rülicke et al, 1998) and the red jungle fowl (Løvlie et al, 2013), but the mechanisms by which such a non-random gamete fusion occurs are yet unknown. In this study, we observed an MHC class II-based fertilization success, but our data suggests that this bias is achieved via mechanisms other than MHC-based sperm velocity in ovarian fluid.…”

“…Potentially, MHC-dependent CFC could also arise after the sperm has entered the egg and before the pronucleus fusion (Yeates et al, 2009). MHC-based CFC was uncovered in the red jungle fowl (Løvlie et al, 2013) and in vitro fertilization experiments in MHC-congenic mice revealed an MHC-dependent gamete fusion (Wedekind et al, 1996;Rülicke et al, 1998).…”

A cry for help: female distress calling during copulation is context dependent

“…Birkhead, 2000; but see Pizzari et al, 2004;Løvlie et al, 2013). As a result, female mating preferences in the fowl are likely to exaggerate the intersexual conflict between subdominant males and females, with the potential to trigger selection for further counteradaptations in both sexes.…”

Sexual selection and the evolutionary dynamics of the major histocompatibility complex

“…Post-copulatory sexual selection may have an important influence on MHC allelic dynamics [21], even in species that show no MHC-based preferences during mate choice.…”

“…Studies of congenic populations of laboratory mice provided the first evidence that individuals could discriminate MHC-based odour cues and use this information when making reproductive decisions [19,20], potentially enhancing genetic diversity via MHCbased disassortative mating. Selection may also extend after mating, via sperm competition and/or cryptic choice prior to fertilization [21,22] and/or sperm -egg incompatibility associated with MHC genotype (reviewed in [23]). …”