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.

Fig. 1.

Relation between body weight and testes weight in murid rodents (r² = 0.4587, n = 31, P < 0.0001). Filled circles: Apodemus agrarius, Apodemus flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Mus bactrianus, Mus castaneus, Mus cookii, Mus domesticus, Mus macedonicus, Notomys alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys natalensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsburgensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys shortridgei, Rattus exulans, Rattus norvegicus, and Rattus rattus. Data are from Kenagy and Trombulak (35), except for those of Mus species, which are our own. Open circles: M. musculus, M. pahari, M. spicilegus, and M. spretus.

Fig. 2.

Relative testes size, proportion of capacitated spermatozoa, and acrosome reaction in response to progesterone in four murid species. (a) Relative testes size. (b) Proportion of spermatozoa showing the “B” pattern, indicative of capacitated, acrosome-intact spermatozoa, at the point of maximum capacitation. (c) Acrosome reaction in response to stimulation with progesterone. Spermatozoa were incubated under capacitating conditions until the time point of maximum capacitation and were then exposed to 15 μM progesterone for 30 min or its solvent (DMSO) as a control. The proportion of spermatozoa responding to progesterone was calculated by subtracting the control values (untreated spermatozoa) from those found in spermatozoa exposed to progesterone. (d) Proportion of spermatozoa undergoing the acrosome reaction in response to stimulation with progesterone in relation to the proportion of capacitated spermatozoa. The proportion of spermatozoa responding to progesterone was calculated by subtracting control values (i.e., untreated spermatozoa). The proportion of capacitated spermatozoa was that observed at the time point of maximal capacitation (“B” pattern). Results are means ± SEM of three independent experiments with spermatozoa from different males (n = 3).