Comparative Analysis of Testis Protein Evolution in Rodents

Abstract

Genes expressed in testes are critical to male reproductive success, affecting spermatogenesis, sperm competition, and sperm-egg interaction. Comparing the evolution of testis proteins at different taxonomic levels can reveal which genes and functional classes are targets of natural and sexual selection and whether the same genes are targets among taxa. Here we examine the evolution of testis-expressed proteins at different levels of divergence among three rodents, mouse (Mus musculus), rat (Rattus norvegicus), and deer mouse (Peromyscus maniculatus), to identify rapidly evolving genes. Comparison of expressed sequence tags (ESTs) from testes suggests that proteins with testis-specific expression evolve more rapidly on average than proteins with maximal expression in other tissues. Genes with the highest rates of evolution have a variety of functional roles including signal transduction, DNA binding, and eggsperm interaction. Most of these rapidly evolving genes have not been identified previously as targets of selection in comparisons among more divergent mammals. To determine if these genes are evolving rapidly among closely related species, we sequenced 11 of these genes in six Peromyscus species and found evidence for positive selection in five of them. Together, these results demonstrate rapid evolution of functionally diverse testis-expressed proteins in rodents, including the identification of amino acids under lineage-specific selection in Peromyscus. Evidence for positive selection among closely related species suggests that changes in these proteins may have consequences for reproductive isolation.

Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions

“…This can reveal whether different family members are coopted for similar functions in different species. Studies using these approaches and including multigene comparisons report a higher average rate of evolution for testis-biased or testis-specific genes in chimpanzees (in which sperm competition is more intense) in comparison to humans (Wong 2010; see Turner and Hoekstra 2008 for a similar comparison in rodents).…”

Effects of different kinds of essentiality on sequence evolution of human testis proteins

“…In particular, male reproductive proteins have been described to evolve rapidly (see, e.g., refs 11 and 12). Furthermore, genes with testis-specific expression evolve at overall higher rates relative to female-specific genes or those unrelated to reproduction in Drosophila 13 and relative to genes with expression maxima in other rodent tissues14. Thereby, rate acceleration of male reproductive proteins is assumed to be driven by different forms of postmating sexual selection, such as sperm competition and sexual conflict (see, e.g., refs 14 and 15).…”

The Genetics of Postmating, Prezygotic Reproductive Isolation Between Drosophila virilis and D. americana

“…In recent years, many studies have also documented strong signatures of positive selection in the rapid evolution of reproductive genes (e.g., Haerty et al 2007;Turner et al 2008; reviewed in Swanson and Vacquier 2002;Clark et al 2006). For internally fertilizing species, coevolution between the female reproductive tract and the male ejaculate is particularly dynamic (Pitnick et al 2007).…”