Extra‐pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean

Abstract

Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen‐mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra‐pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed brood paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra‐pair males in a nonrandom, self‐matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a compatible genes model for extra‐pair mate choice where the optimal allelic diversity is intermediate, not maximal. This golden mean presumably reflects a trade‐off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra‐pair mating is adaptive through altered genetic constitution in offspring.

MHC-Based Mate Choice in Wild Golden Snub-Nosed Monkeys

“…The functional loci of the MHC are thus more likely to be the targets of female mate choice in R. roxellana. Several studies have also reported evidence for intermediate dissimilarity choice at MHC loci (Bonneaud et al, 2006;Forsberg et al, 2007;Eizaguirre et al, 2009;Rekdal et al, 2019). This concurs with mate choice for MHC dissimilarity to produce offspring that can cope with a wide-range of pathogens.…”

“…These genes are involved in the recognition and presentation of intracellular (such as viruses) and extracellular (such as bacteria) antigens to T-cells, thereby contributing to a host immune response to pathogen attack (Doherty and Zinkernagel, 1975;Bernatchez and Landry, 2003). Several studies have shown that MHC genes are important for mate choice in several vertebrate species, with females not only benefiting directly by mating with "healthy" males (i.e., females may be less likely to be infected with pathogens from their mates) but also indirectly by producing offspring with enhanced capacity to fight pathogen infection (Landry et al, 2001;Richardson et al, 2005;Santos et al, 2017;Rekdal et al, 2019). MHC genes thus make an ideal study system to enable the identification of specific functional loci effects of female mate choice (Penn and Potts, 1999;Milinski, 2006;Schwensow et al, 2008a,b;Wedekind and Evanno, 2010).…”

Male validation factor for three-spined stickleback (Gasterosteus aculeatus) mate choice likely evolutionarily conserved since 50 thousand years

“…mice (Leinders-Zufall et al 2004), fish (Milinski et al 2005) and humans (Milinski et al 2013). Each individual carries only a small, optimal number of MHC alleles (Wegner et al 2003;Forsberg et al 2007;Rekdal et al 2019). This optimum is a tradeoff between having many alleles for maximizing disease detection and having few alleles to reduce negative selection of T-cells, which are necessary for fighting the detected disease (Janeway et al 2001;Wölfing et al 2008).…”

Data_Sheet_1.docx

“…A role for the MHC in mate choice has been found in a variety of vertebrate taxa (such as fish, reptiles, birds, rodents, and primates; Miller et al, 2009;Setchell et al, 2011;Evans et al, 2012;Paula Cutrera et al, 2012;Rekdal et al, 2019). There are three not necessarily mutually exclusive mechanisms by which MHC is relevant to mate choice.…”

“…The chooser will benefit by producing offspring of intermediate rather than maximal MHC genetic diversity. This avoids any costs associated with excessive outbreeding depression, and/or locally adapted gene complexes affecting the immune systems of offspring being disrupted, and also avoids the consumption of mature T-cell repertoire in offspring with high MHC diversity (Luscinia svecica, Rekdal et al, 2019;Mandrillus sphinx, Setchell et al, 2016). (2) Choice for heterozygosity (diversity), in which heterozygous mating partners are preferred.…”