Abstract
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.
Highlights
Sperm competition is a powerful selective force that has shaped male reproductive behavior, physiology, reproductive tract morphology, and gamete phenotype [1,2,3]
Despite being phylogenetically very close, muroid species examined in this study showed high variability of testes masses, despite much lower levels of variation in body mass
Major differences were found in terms of both sperm numbers and traits that determine ejaculate quality which were associated with levels of sperm competition in phylogenetically-controlled analyses
Summary
Sperm competition is a powerful selective force that has shaped male reproductive behavior, physiology, reproductive tract morphology, and gamete phenotype [1,2,3]. A widespread response to an increase in levels of sperm competition is an increase in testes mass relative to body mass [2,3,9,10]. Increases in relative testes mass often involve both an increase in the amount of sperm producing tissue and in the efficiency per unit of tissue [14]. This results in higher sperm numbers in sperm reserves, which translates into more sperm per ejaculate [15,16]. Theoretical models suggest that males with more sperm should gain a greater share of paternity when mechanisms of sperm competition resemble a raffle [18], and experimental studies have shown that males which transfer more sperm per ejaculate gain more fertilizations (see reviews in [1])
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