2006Proceedings of the National Academy of SciencesOpen access

Sperm competition enhances functional capacity of mammalian spermatozoa

Montserrat Gomendio, Juan Martín-Coello, Cristina Crespo, Concepción Magaña, Eduardo R. S. Roldán

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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.

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What this paper is about

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.

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Available 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.

Key concepts: Polyspermy, Sperm, Sperm competition, Human fertilization, Biology, Capacitation, Competition (biology), Population

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