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

Abstract

The genes of the major histocompatibility complex (MHC) are an important component of the vertebrate immune system and play a significant role in mate choice in many species. However, it remains unclear whether female mate choice in non-human primates is based on specific functional genes and/or genome-wide genes. The golden snub-nosed monkey (Rhinopithecus roxellana) lives in a multilevel society, which consists of several polygynous one-male-several-female units. Although adult females tend to mainly socialize with one adult male, females often initiate extra-pair copulations with other males resulting in a high proportion of offspring being fathered by extra-pair males. We investigated the effects of adaptive MHC genes and neutral microsatellites on female mate choice in a wild R. roxellana population. We sequenced 54 parent-offspring triads using two MHC class II loci (Rhro-DQA1 and Rhro-DQB1) and 20 microsatellites from 3 years of data. We found that the paternities of offspring were non-randomly associated with male MHC compositions not microsatellite genotypes. Our study showed that the fathers of all infants had significantly less variance for several estimates of genetic similarity to the mothers compared with random males at both MHC loci. Additionally, the MHC diversity of these fathers was significantly higher than random males. We also found support for choice based on specific alleles; compared with random males, Rhro-DQA1∗ 05 and Rhro-DQB1∗ 08 were more common in both the OMU (one-male unit) males and the genetic fathers of offspring. This study provides new evidence for female mate choice for MHC-intermediate dissimilarity (rather than maximal MHC dissimilarity) and highlights the importance of incorporating multiple MHC loci and social structure into studies of MHC-based mate choice in non-human primates.

Social and paternal female choice for male MHC genes in golden snub‐nosed monkeys (Rhinopithecus roxellana)

“…Thus, rather than seeking paternal mates with maximal MHC dissimilarity (e.g., Gessner et al, 2017; Schwensow, Eberle, & Sommer, 2008; Strandh et al, 2012), female golden snub‐nosed monkeys tend to prefer paternal mates of intermediate MHC dissimilarity. This is consistent with another recent work on R. roxellana based on two MHC loci (Zhang et al, 2020). Similar preferences for intermediate MHC dissimilarity are also present in brown trout Salmo trutta L. (Forsberg et al, 2007), three‐spined sticklebacks Gasterosteus aculeatus (Eizaguirre et al, 2009), house sparrows Passer domesticus (Bonneaud et al, 2006), and bluethroats Luscinia svecica (Rekdal et al, 2019), and will produce offspring with intermediate MHC diversity, rather than maximum diversity.…”

Paternity data reveal high MHC diversity among sires in a polygynandrous, egalitarian primate

“…We first tested whether females reproduced with males who possessed a greater number of MHC DRB1 alleles than expected by chance (Prediction 1), which would be consistent with female mate choice for males with higher MHC diversity. This idea has been supported in several studies of nonhuman primates, humans and vertebrates in general [50,51]. Second, we tested whether females reproduced with males with whom, on average, they shared fewer MHC DRB1 alleles (Prediction 2a) or who had more 'distinct' MHC DRB1 alleles, i.e.…”

Relationship between genome‐wide and MHC class I and II genetic diversity and complementarity in a nonhuman primate

“…Third, diversity at different MHC classes does not appear to be correlated, suggesting that “allele optimizing” strategies may occur within, not between, MHC class types. Nonetheless, evidence of mate choice prioritizing immunogenetic optimality has been observed in multiple species, including the three‐spined stickleback ( Gasterosteus aculeatus ; Milinski et al, 2005 ), ring‐necked pheasant ( Phasianus colchicums ; Baratti et al, 2012 ), and golden snub‐nosed monkey (Zhang et al, 2020 ), among others. Further investigation of how diversity at class I and II loci interact and are coadapted for particular pathogen environments will be needed to understand the causes and consequences of diversity at these different class types.…”

“…As a consequence, mate choice favoring partners with high genome‐wide diversity may or may not reinforce mate choice favoring genetic diversity at the MHC. Some mate choice studies have attempted to address this potentially confounding interaction between genome‐wide and MHC diversity by investigating how MHC heterozygosity and complementary relate to genome‐wide heterozygosity and kinship estimated using a small number of microsatellites (5 loci: Landry et al, 2001 ; 7 loci: Schwensow et al, 2008 ; 16 loci: Huchard et al, 2010 ; 20 loci: Zhang et al, 2020 ). Although microsatellites perform well in a variety of analytical contexts, genotyping at a small number of microsatellites can be an unreliable proxy of overall genomic heterozygosity (Väli et al, 2008 ), which may be influenced by population history and degree of microsatellite polymorphism (Miller et al, 2014 ).…”