Sexual Selection Halts the Relaxation of Protamine 2 among Rodents

Abstract

Sexual selection has been proposed as the driving force promoting the rapid evolutionary changes observed in some reproductive genes including protamines. We test this hypothesis in a group of rodents which show marked differences in the intensity of sexual selection. Levels of sperm competition were not associated with the evolutionary rates of protamine 1 but, contrary to expectations, were negatively related to the evolutionary rate of cleaved- and mature-protamine 2. Since both domains were found to be under relaxation, our findings reveal an unforeseen role of sexual selection: to halt the degree of degeneration that proteins within families may experience due to functional redundancy. The degree of relaxation of protamine 2 in this group of rodents is such that in some species it has become dysfunctional and it is not expressed in mature spermatozoa. In contrast, protamine 1 is functionally conserved but shows directed positive selection on specific sites which are functionally relevant such as DNA-anchoring domains and phosphorylation sites. We conclude that in rodents protamine 2 is under relaxation and that sexual selection removes deleterious mutations among species with high levels of sperm competition to maintain the protein functional and the spermatozoa competitive.

Sexual selection and the adaptive evolution of PKDREJ protein in primates and rodents

“…It is possible that the adaptive evolution of PKDREJ is a generalized phenomenon across rodents, but the high degree of conservation of a large portion of the gene makes it difficult to detect positive selection when very closely related species are compared (Anismova et al, 2001;Zhang et al, 2005). A similar pattern was observed in previous work analysing the evolution of protamine sequences in murids (Martín-Coello et al, 2009) and cricetids (Lüke et al, 2011). An alternative explanation could be that positive selection is limited to the cricetid clade.…”

“…The evolutionary rate of Pkdrej for each species was then calculated by comparing dN and dS values from the root of the phylogeny to the terminal branch giving an v ratio from the root. In this way, the total accumulated selective pressures during the evolution of the Pkdrej gene are accounted for, which is more suitable for testing associations with phenotypic data as it reflects the entire phenotypic evolution from the common ancestor (Lüke et al, 2011;Montgomery et al, 2011). In addition, estimating the rate of evolution since the last common ancestor forces that all branches have the same length and therefore the analysis is not subject to temporal effects on v (Wolf et al, 2009).…”

“…Evidence for post-copulatory sexual selection influencing the molecular evolution of reproductive genes is limited and often controversial in rodents (Ramm et al, 2008;Lüke et al, 2011). A rodent gene coding for an ejaculate protein involved in the formation of the copulatory plug (Svs2) was shown to exhibit signs of positive selection in species with high levels of sperm competition (Ramm et al, 2008).…”

“…A rodent gene coding for an ejaculate protein involved in the formation of the copulatory plug (Svs2) was shown to exhibit signs of positive selection in species with high levels of sperm competition (Ramm et al, 2008). Evolutionary analyses of protamines, a family of nuclear proteins involved in condensing sperm chromatin during spermiogenesis, revealed a negative correlation between rate of divergence in Prm2 and sperm competition intensity, suggesting that sexual selection may have a role in halting the degeneration of this protein (Lüke et al, 2011). The findings in the present study would thus represent the first evidence in rodents of adaptive evolution of an integral sperm protein associated with sexual selection.…”

Sexual selection on protamine and transition nuclear protein expression in mouse species

“…A number of studies have found a positive relationship between sequence divergence of these genes and levels of sperm competition, and several such genes show evidence of positive selection in coding regions ( [17][18][19][20][21], but see [22,23]). However, a positive correlation between sequence divergence in the promoter region of protamine 2 and relative levels of sperm competition in house mice and their close relatives [24] suggests that regulatory changes may also contribute to species differences in sperm competitive ability.…”