Of mice and sperm.

W hen females are sexually promiscuous, the ejaculates of different males may compete for the fertilization of a set of ova, a process known as sperm competition. In internally fertilizing species, potential for sperm competition occurs whenever the ejaculates of different males cooccur in the female reproductive tract at the time of ovulation. Sperm competition is now recognized as a powerful agent of evolutionary change, and the signal of its selective pressure is being detected on a number of male physiological and behavioral traits (1, 2). One of the major determinants of the outcome of sperm competition is the relative numerical representation of different ejaculates at the time of fertilization. All else being equal, the male that inseminates more sperm into a female has a fertilizing edge over his competitors (1, 3). The rate of spermatogenesis is determined by gonadal mass, and under more intense sperm competition we would expect males to grow relatively large testicles to inseminate more sperm. Evidence that sperm competition favors the evolution of larger testes relative to body mass (gonadosomatic index) comes from multiple comparative and experimental evolution studies across a number of taxa (1, 4–7). In addition to the number of sperm inseminated, the fertilizing efficiency of sperm also plays a critical role in sperm competition (8). Therefore, traits associated with the fertilizing performance of an ejaculate are also expected to evolve in response to sperm competition. The work by Gomendio et al. (9) in this issue of PNAS reveals that sperm competition may also have shaped the evolution of sperm function in eutherian mammals. Fertilization in eutherian mammals is a complicated business. After ejaculation, spermatozoa face two hierarchical challenges. First, sperm must undergo a process of maturation in the female uterus and oviduct. This process is known as capacitation and is triggered by the exogenous biochemical milieu of the female tract, as sperm are transported to the ampulla of the fallopian tube, where fertilization occurs. Capacitation involves a number of biochemical changes that prepare the spermatozoon for a process of specialized exocytosis known as acrosome reaction (10). The acrosome reaction results in the progressive loss of the plasma membrane from its acrosomal cap and the release of the hydrolytic enzymes stored in the acrosomal granule, which enable sperm to penetrate the zona pellucida of the ovum. Acrosome reaction must be timed precisely, because both premature and delayed acrosome reaction will prevent sperm from penetrating the granulose cells accumulated around the ovum (cumulus oophorus) and adhering to the zona pellucida (10). The timing of acrosome reaction is modulated by sperm exposure to the progesterone contained in the cumulus oophorus (11). Capacitation is also associated with a state of ‘‘hyperactivation’’ characterized by a drastic change in sperm motility, which may help capacitated sperm to free themselves from the epithelium of the female reproductive tract and is essential to overcome the resistance of the zona pellucida and thus to penetrate the ovum (10, 12). Once they are capacitated, sperm display increased metabolism and energy expenditure, which may reduce sperm life expectancy because of increased oxidative stress (13). Premature capacitation relative to ovulation may thus result in a drastic loss of fertilizing efficiency of an ejaculate. Nevertheless, the rate at which sperm reach capacitation and the proportion of capacitated sperm that undergo acrosome reaction vary widely across species, and the significance of this variation has remained largely unexplained (10). Gomendio et al. (9) tested the idea that variation in capacitation and acrosome reaction rates across species of murid rodents may be explained by sperm competition. Murids are an appropriate eutherian taxon for the study of sperm competition because, although little is known about the mating behavior of most species, the high interspecific variation in male gonadosomatic index values indicates different levels of sperm competition across species. Gomendio et al. (9) selected four species of the Mus genus in which mean testicular mass ranged from 0.4% male body mass in Mus pahari to 3% in Mus spicilegus, with intermediate values for Mus spretus (1.7%; Fig. 1A) and Mus musculus (0.6%). As expected, the rate of sperm production of a species was predicted by its gonadosomatic index. The authors (9) investigated whether sperm function also covaried with male gonadosomatic index. The study of sperm capacitation was catalyzed in 1963, when Yanagimachi and Chang first demonstrated that capacitation can be induced in vitro (10). Gomendio et al. (9) adopted a similar approach to study sperm capacitation. The rate of capacitation is not constant and typically displays a peak: the higher the peak in capacitation rate, the more synchronous sperm capacitation occurs in a sperm population. The authors (9) analyzed the proportion of sperm that underwent capacitation in vitro within a time window