Sperm competition enhances functional capacity of mammalian spermatozoa

Abstract

When females mate promiscuously, sperm from rival males compete within the female reproductive tract to fertilize ova. Sperm competition is a powerful selective force that has shaped sexual behavior, sperm production, and sperm morphology. However, nothing is known about the influence of sperm competition on fertilization-related processes, because it has been assumed that sperm competition only involves a race to reach the site of fertilization. We compared four closely related rodent species with different levels of sperm competition to examine whether there are differences in the proportion of spermatozoa that become ready to interact with the ovum (''capacitated'') and in the proportion of spermatozoa that experience the acrosome reaction in response to a natural stimulant. Our results show that differences between species in levels of sperm competition were associated with the proportion of spermatozoa that undergo capacitation and with the proportion of spermatozoa that respond to progesterone, an ovum-associated signal. Sperm competition thus favors a larger population of spermatozoa that are competent to fertilize, and spermatozoa that are more sensitive to the signals emitted by the ovum and that may penetrate the ova vestments more rapidly. These results suggest that, contrary to previous assumptions, competition between spermatozoa from rival males continues at the site of fertilization. These findings may have further evolutionary implications because the enhanced competitiveness of spermatozoa during fertilization may increase the risk of polyspermy to females. This could lead to antagonistic coevolution between the sexes and may contribute to the explanation of the rapid divergence observed in fertilization-related traits.sperm function ͉ capacitation ͉ acrosome reaction fertilization ͉ antagonistic coevolution

A polycystin-1 controls postcopulatory reproductive selection in mice

“…In contrast, in natural populations outside the laboratory, female mice are polyandrous and mate with multiple males during an estrus cycle (24)(25)(26). A second breeding protocol was used to mimic these aspects of mating behavior.…”

Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species

“…This may be realized by an increase of sperm producing tissue within the testis as observed in birds [72]. Additionally, also ejaculate quality may be increased, but in rodents such sperm competition metrics are typically strongly related to RTS [73][74][75][76].…”

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

“…These three species have been characterized as a good model for studies on sperm competition in rodents, representing low, intermediate and high levels of sperm competition, respectively [6]. For each male, we incubated spermatozoa from one cauda epididymis under non-capacitating conditions (medium mT-H, under air, at 378C) and spermatozoa from the other cauda under capacitating conditions (medium mT-HB, under 5% CO 2 /air, at 378C).…”

“…High levels of sperm competition are associated with an increase in the production, storage and allocation of spermatozoa, as well as with enhanced sperm function [3][4][5]. In rodents, high levels of sperm competition lead to a higher proportion of spermatozoa that are morphologically normal, motile and capable of reaching and fertilizing the ovum [6,7], as well as in modifications in sperm dimensions that may result in improvements in sperm movement [8,9]. In many taxa, sperm swimming velocity, an important feature of sperm function, is also higher in those species that experience high levels of sperm competition [9][10][11][12].…”

“…Hyperactivated motility, because of its presumed increase in energetic demands, could lead to an enhanced production of ROS and thus increased sperm DNA damage. To test this prediction, we incubated sperm cells from three species of mice from the genus Mus that differ in their levels of sperm competition [6] under non-capacitating and capacitating conditions, and quantified sperm DNA integrity.…”