Abstract
Little is known about the genetic basis of evolutionary changes in sperm phenotype. Postcopulatory sexual selection is associated with differences in protamine gene sequences and promoters and is a powerful force acting on sperm form and function, although links between protamine evolution and sperm phenotype are scarce. Protamines are involved in sperm chromatin condensation, and protamine deficiency negatively affects sperm morphology and male fertility, thus suggesting that they are important for sperm design and function. We examined changes in protamine genes and sperm phenotype in rodents to understand the role of sexual selection on protamine evolution and sperm design. We performed a genotype-phenotype association study using root-to-tip dN/dS (nonsynonymous/synonymous substitutions rate ratio) to account for evolutionary rates and phylogenetic generalized least squares analyses to compare genetic and morphometric data. Evolutionary rates of protamine 1 and the protamine 2 domain cleaved off during chromatin condensation correlated with head size and elongation. Protamine 1 exhibited restricted positive selection on some functional sites, which seemed sufficient to preserve its role in head design. The cleaved-protamine 2, whose relaxation is halted by sexual selection, seems to ensure small, elongated heads that would make sperm more competitive. No association existed between mature-protamine 2 and head phenotype, suggesting little involvement during chromatin condensation and a likely role maintaining the condensed state. Our results suggest that evolutionary changes in protamines could be related to complex developmental modifications in the sperm head. This represents an important step toward understanding the role of changes in gene coding sequences in the divergence of germ cell phenotype.
Highlights
Postcopulatory sexual selection, in the form of sperm competition, is an evolutionary force known to drive rapid adaptation of reproductive traits [1,2,3,4] and that has beenReceived: 13 November 2013
Because total sperm length varies greatly among these species, and drag resulting from head size should be analyzed taking into account the length of the flagellum [17], relative head length (HL) and head width (HW) were each calculated as percentages of total sperm length
We examined genetic-morphometric associations by analyzing differences in protamine gene sequences and sperm head size and elongation with the aim of understanding the role of sperm competition on reproductive trait evolution
Summary
Postcopulatory sexual selection, in the form of sperm competition, is an evolutionary force known to drive rapid adaptation of reproductive traits [1,2,3,4] and that has beenReceived: 13 November 2013. Postcopulatory sexual selection, in the form of sperm competition, is an evolutionary force known to drive rapid adaptation of reproductive traits [1,2,3,4] and that has been. Ó 2014 by the Society for the Study of Reproduction, Inc. eISSN: 1529-7268 http://www.biolreprod.org ISSN: 0006-3363 linked to rapid diversification of coding sequences of the socalled reproductive proteins [5, 6]. Reproductive proteins include those that act following copulation and that mediate gamete usage, storage, signal transduction, and fertilization [5]. The genetic basis of evolutionary changes in sperm phenotype has, so far, received very limited attention in mammals
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