Sexual Selection Shapes Seminal Vesicle Secretion Gene Expression in House Mice

Abstract

Reproductive proteins typically have high rates of molecular evolution, and are assumed to be under positive selection from sperm competition and cryptic female choice. However, ascribing evolutionary divergence in the genome to these processes of sexual selection from patterns of association alone is problematic. Here, we use an experimental manipulation of postmating sexual selection acting on populations of house mice and explore its consequences for the expression of seminal vesicle secreted (SVS) proteins. Following 25 generations of selection, males from populations subjected to postmating sexual selection had evolved increased expression of at least two SVS genes that exhibit the signature of positive selection at the molecular level, SVS1 and SVS2. These proteins contribute to mating plug formation and sperm survival in the female reproductive tract. Our data thereby support the view that sexual selection is responsible for the evolution of these seminal fluid proteins.

The hidden ageing costs of sperm competition

“…Ramm et al 2005) and experimental (e.g. Simmons et al ., 2020) data pointing towards the importance of increased allocation to seminal fluid under heightened levels of sperm competition. Interestingly, the female ageing cost of repeated exposure to male seminal fluid content has been studied extensively (see Box 1).…”

Seminal fluid and accessory male investment in sperm competition

“…Experimental evolution approaches that seek to isolate the effect of sperm competition level on seminal fluid investment may be especially valuable here. For example, enforced monogamy led to a decline in the expression of many seminal fluid genes in Drosophila [51,52] as well as that of two major seminal fluid components, SVS1 and SVS2, in house mice [53]. In both cases, this was accompanied by corresponding reductions in sperm competitiveness, for which these expression changes may be at least partially responsible [52,54].…”

High rates of evolution preceded shifts to sex-biased gene expression inLeucadendron, the most sexually dimorphic angiosperms

“…In contrast to previous work in plants and animals, the phylogenetic context of our sampling allowed us to ask whether rates of expression evolution accelerated for genes once they became sex-biased, or whether expression levels were already evolving rapidly before they became sexbiased. The former possibility would be consistent with the outcome of sex-specific (or sexual) selection, for example (Pointer et al 2013;Hollis et al 2014;Immonen et al 2014;Simmons et al 2020), whereas the latter possibility would be more consistent with reduced functional constraints of expression levels for sex-biased genes, i.e., they evolve more quickly because they can do so with impunity (Orr 2000;Papakostas et al 2014), and hence then are freer to become sex-biased, too. We thus compared rates of expression evolution between unbiased genes and SBGs.…”

“…Comparisons of DNA sequences and gene expression phenotypes between species with contrasting degrees of sexual dimorphism can provide important evidence to evaluate this theory, because past phases of selection or drift can be diagnosed by characteristic patterns (Ranz et al 2003;Khaitovich et al 2005;Ellegren and Parsch 2007;Voolstra et al 2007;Harrison et al 2015;Naqvi et al 2019). Under the hypotheses that sex-related adaptation drives SBGE, one would expect that sex-biased genes show elevated rates of amino acid substitution and faster rates of expression divergence between species (Pointer et al 2013;Hollis et al 2014;Immonen et al 2014;Grath and Parsch 2016;Simmons et al 2020). Tests of such predictions have provided evidence consistent with this idea in many animals (Ellegren and Parsch 2007;Harrison et al 2015;Grath and Parsch 2016), but results have been mixed or negative in plants (Ellegren and Parsch 2007;Muyle 2019).…”