The evolution of sperm competition genes: The effect of mating system on levels of genetic variation within and between species

Abstract

It is widely established that proteins involved in reproduction diverge between species more quickly than other proteins. For male sperm proteins, rapid divergence is believed to be caused by post-copulatory sexual selection and/or sexual conflict. Here, we derive the expected levels of gene diversity within populations and divergence between them for male sperm protein genes evolving by post-copulatory, pre-zygotic fertility competition, i.e. the function imputed for some sperm and seminal fluid genes. We find that, at the mutation-selection equilibrium, both gene diversity within species and divergence between them are elevated relative to genes with similar selection coefficients expressed by both sexes. We show that their expected level of diversity is a function of the harmonic mean number of mates per female which affects the strength of fertility selection stemming from male-male sperm competition. Our predictions provide a null hypothesis for distinguishing between other selective hypotheses accounting for the rapid evolution of male reproductive genes.

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

“…The current evidence is unclear whether rapid rates of evolution for sex-biased genes observed in other organisms is due to positive selection (Proschel et al 2006), perhaps related to sexual selection or sperm competition (Ellegren and Parsch 2007), or is due to relaxed constraint and genetic drift (Harrison et al 2015; Dapper and Wade 2016). We used codon-bias, tissue-specificity and signatures of selection on coding sequence to differentiate these two potential forces.…”

“…This complex pattern may vary across distantly related groups, explaining why work in Drosophila has recovered stronger signatures of selection in male-biased genes (Proschel et al 2006), whereas studies in adult birds (Harrison et al 2015) and humans (Gershoni and Pietrokovski 2014) reveals patterns more consistent with relaxed evolutionary constraint and genetic drift. Given this complex, clade-specific pattern, as well as recent concerns about how expression-bias might alter mutation-selection dynamics (Dapper and Wade 2016), data from more species are needed to resolve this debate. …”

“…Although work in Drosophila has shown that male-biased genes more often exhibit a signature of adaptive evolution (Proschel et al 2006), evidence from birds (Harrison et al 2015) and humans (Gershoni and Pietrokovski 2014) indicate relaxed constraint might be driving rapid rates of evolution. Additionally, there have been recent concerns about how expression-bias might alter mutation-selection dynamics (Dapper and Wade 2016), leading to the fixation of mildly deleterious alleles in strongly male-biased genes (Gershoni and Pietrokovski 2014). Data from more species are needed to resolve this debate.…”

Population genetics of sexual conflict in the genomic era

“…3). Such loci are under positive or purifying selection in one sex but experience the mutational input from both, which will lead to more genetic diversity than expected [49][50][51] . Consistent with this notion, recent work suggests that differences in allele frequency between males and females in humans are indeed a result of sex-specific survival 52 .…”

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

“…Because fertility was assayed at the level of males, not gametes, we used male trait means in our analyses of selection. Conceptually, doing so assumes that sperm phenotypes are determined more by the diploid genomes of males than by the haploid genomes of sperm, as seems to be the case for most species [44]. Statistically, doing so assumes that trait values are fixed variables measured without error, which is expected to bias our estimates of selection towards zero, but does not bias the hypothesis tests of these coefficients that are our focus here [45].…”