Female Promiscuity Is Positively Associated With Neutral and Selected Genetic Diversity in Passerine Birds

Abstract

Passerine birds show large interspecific variation in extrapair paternity rates. There is accumulating evidence that such promiscuous behavior is driven by indirect, genetic benefits to females. Sexual selection theory distinguishes between two types of genetic benefits, additive and nonadditive effects, mediated by preferences for good and compatible genes, respectively. Good genes preferences should imply directional selection and mating skew among males, and thus reduced genetic diversity in the population.In contrast, compatible genes preferences should give balancing selection that retains genetic diversity. Here, we test how well these predictions fit with patterns of variation in genetic diversity and promiscuity levels among passerine birds. We found that more promiscuous species had higher nucleotide diversity at autosomal introns, but not at Z-chromosome introns. We also found that major histocompatibility complex (MHC) class IIB alleles had higher sequence diversity, and therefore should recognize a broader spectrum of pathogens, in more promiscuous species. Our results suggest that female promiscuity targets a multitude of autosomal genes for their nonadditive, compatibility benefits. Also, as immunity genes seem to be of particular importance, we hypothesize that interspecific variation in female promiscuity among passerine birds has arisen in response to the strength of pathogen-mediated selection. K E Y W O R D S :Balancing selection, compatible genes, extrapair paternity, MHC, pathogen-mediated selection, sperm competition.

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

“…Our finding of a weak negative relationship between parasite richness and relative testes size, however, is not consistent with this hypothesis. Importantly, each of these mechanisms predicts that greater promiscuity will lead to greater genetic diversity, a result already observed for MHC and neutral genetic diversity across passerine birds [81]. Our analysis did not support an interactive effect between parasite richness and relative testes size, as might be expected if both high parasite pressure and the potential for mate choice were necessary to drive high MHC diversity.…”

Migration distance is positively associated with sex-linked genetic diversity in passerine birds

“…Female promiscuity, on the other hand, was 173 positively associated with autosomal genetic diversity, irrespective of the variation in 174 migration distance. Hence, we can conclude that, in our data set, migration distance is not a 175 confounding variable for the relationship between female promiscuity and autosomal diversity 176 reported in a previous study (GOHLI et al, 2013). Our results indicate that some variable, 177 which is associated with migration distance, affects Z-linked diversity specifically.…”

No evidence for MHC class I‐based disassortative mating in a wild population of great tits

“…For instance, Gohli et al . () have recently shown a positive relationship between MHC class IIB functional diversity and population promiscuity in a comparative analysis of passerine birds and suggested that female promiscuity is a driving force maintaining MHC genetic diversity through balancing selection (but see Spurgin, ). Evidence for MHC‐based extra‐pair copulations has been provided in several wild bird studies (Freeman‐Gallant et al ., ; Richardson et al ., ; Promerová et al ., ; but see Bollmer et al ., ).…”