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Structural evolution of CatSper1 in rodents is influenced by sperm competition, with effects on sperm swimming velocity.

ABSTRACT: BACKGROUND: Competition between spermatozoa from rival males for success in fertilization (i.e., sperm competition) is an important selective force driving the evolution of male reproductive traits and promoting positive selection in genes related to reproductive function. Positive selection has been identified in reproductive proteins showing rapid divergence at nucleotide level. Other mutations, such as insertions and deletions (indels), also occur in protein-coding sequences. These structural changes, which exist in reproductive genes and result in length variation in coded proteins, could also be subjected to positive selection and be under the influence of sperm competition. Catsper1 is one such reproductive gene coding for a germ-line specific voltage-gated calcium channel essential for sperm motility and fertilization. Positive selection appears to promote fixation of indels in the N-terminal region of CatSper1 in mammalian species. However, it is not known which selective forces underlie these changes and their implications for sperm function. RESULTS: We tested if length variation in the N-terminal region of CatSper1 is influenced by sperm competition intensity in a group of closely related rodent species of the subfamily Murinae. Our results revealed a negative correlation between sequence length of CatSper1 and relative testes mass, a very good proxy of sperm competition levels. Since CatSper1 is important for sperm flagellar motility, we examined if length variation in the N-terminus of CatSper1 is linked to changes in sperm swimming velocity. We found a negative correlation between CatSper1 length and several sperm velocity parameters. CONCLUSIONS: Altogether, our results suggest that sperm competition selects for a shortening of the intracellular region of CatSper1 which, in turn, enhances sperm swimming velocity, an essential and adaptive trait for fertilization success.

SUBMITTER: Vicens A

PROVIDER: S-EPMC4041144 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Structural evolution of CatSper1 in rodents is influenced by sperm competition, with effects on sperm swimming velocity.

Vicens Alberto A Tourmente Maximiliano M Roldan Eduardo R S ER

BMC evolutionary biology 20140516

<h4>Background</h4>Competition between spermatozoa from rival males for success in fertilization (i.e., sperm competition) is an important selective force driving the evolution of male reproductive traits and promoting positive selection in genes related to reproductive function. Positive selection has been identified in reproductive proteins showing rapid divergence at nucleotide level. Other mutations, such as insertions and deletions (indels), also occur in protein-coding sequences. These str ...[more]

PMID: 24884901

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Project description:Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An "overall sperm quality" parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert.

Dataset Information

Structural evolution of CatSper1 in rodents is influenced by sperm competition, with effects on sperm swimming velocity.

Publications

Structural evolution of CatSper1 in rodents is influenced by sperm competition, with effects on sperm swimming velocity.

Similar Datasets

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