MBE Advance Access published online on November 20, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm242
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Research Article |
Sexual Selection and the Adaptive Evolution of Mammalian Ejaculate Proteins
1 Mammalian Behaviour & Evolution Group, Faculty of Veterinary Science, University of Liverpool, UK
2 MRC Functional Genetics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, UK
3 Department of Biology, University College London, UK
4 Current address: Institute for Science and Technology in Medicine, School of Medicine, Keele University, UK
Corresponding authors: P. Stockley, Mammalian Behaviour & Evolution Group, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE, UK. Tel: +44 (0)151 794 6103, Fax: +44 (0)151 796 6107, E-mail: p.stockley{at}liverpool.ac.uk R. D. Emes, Institute for Science and Technology in Medicine, Keele University, School of Medicine, Keele Campus, Staffordshire ST5 5BG, UK. Tel: +44(0)1782 584642, Fax: +44(0)1782 584637, E-mail: r.d.emes{at}hfac.keele.ac.uk
Received for publication September 5, 2007. Revision received October 29, 2007. Accepted for publication October 30, 2007.
An elevated rate of substitution characterizes the molecular evolution of reproductive proteins from a wide range of taxa. Although the selective pressures explaining this rapid evolution are yet to be resolved, recent evidence implicates sexual selection as a potentially important explanatory factor. To investigate this hypothesis, we sought evidence of a high rate of adaptive gene evolution linked to post-copulatory sexual selection in muroid rodents, a model vertebrate group displaying a broad range of mating systems. Specifically, we sequenced seven genes from diverse rodents that are expressed in the testes, prostate or seminal vesicles, products of which have the potential to act in sperm competition. We inferred positive Darwinian selection in these genes by estimation of the ratio of non-synonymous (dN, amino acid changing) to synonymous (dS, amino acid retaining) substitution rates (
= dN/dS). Next, we tested whether variation in this ratio among lineages could be attributed to interspecific variation in mating systems, as inferred from the variation in these rodents' relative testis sizes. Four of the seven genes examined (Prm1, Sva, Acrv1 and Svs2, but not Svp2, Msmb or Spink3) exhibit unambiguous evidence of positive selection. One of these, the seminal vesicle-derived protein Svs2, also shows some evidence for a concentration of positive selection in those lineages in which sperm competition is common. However, this was not a general trend among all the rodent genes we examined. Using the same methods, we then re-analyzed previously published data on two primate genes, SEMG1 and SEMG2. Whilst SEMG2 also shows evidence of positive selection concentrated in lineages subject to high levels of sperm competition, no such trend was found for SEMG1. Overall, despite a high rate of positive selection being a feature of many ejaculate proteins, these results indicate that the action of sexual selection potentially responsible for elevated evolutionary rates may be difficult to detect on a gene-by-gene basis. Whilst the extreme diversity of reproductive phenotypes exhibited in nature attests to the power of sexual selection, the extent to which this force predominates in driving the rapid molecular evolution of reproductive genes therefore remains to be determined.
Key Words: adaptive evolution • positive selection • primates • rodents • sexual selection • sperm competition
* These authors contributed equally to this work.