Adaptation to Sperm Competition in Humans

With the recognition, afforded by recent evolutionary science, that female infidelity was a recurrent feature of modern humans’ evolutionary history has come the development of a unique area in the study of human mating: sperm competition. A form of male–male postcopulatory competition, sperm competition occurs when the sperm of two or more males concurrently occupy the reproductive tract of a female and compete to fertilize her ova. Males must compete for mates, but if two or more males have copulated with a female within a sufficiently short period of time, sperm will compete for fertilizations. Psychological, behavioral, physiological, and anatomical evidence indicates that men have evolved solutions to combat the adaptive problem of sperm competition, but research has only just begun to uncover these adaptations. KEYWORDS—sperm competition; anti-cuckoldry; sexual conflict; female infidelity; evolutionary psychology Male flour beetles sometimes fertilize females with a rival male’s sperm. This ‘‘fertilization by proxy’’ occurs when the mating male’s aedeagus (reproductive organ) translocates the sperm of another male into the female’s reproductive tract (Haubruge, Arnaud, Mignon, & Gage, 1999). The sperm of a male that a female has copulated with can adhere to a subsequent male’s aedeagus because these insects’ genitalia have chitinous spines designed to facilitate removal of rival male sperm prior to deposition of self-sperm into a female’s reproductive tract. This phenomenon was predicted and observed by researchers who study sperm competition. Although not yet documented empirically, humans also may experience fertilization by proxy (Gallup & Burch, 2004). More generally, a rapidly growing literature indicates that sperm competition has been an important selection pressure during human evolution. Sperm competition is intrasexual (male–male) competition that occurs after the initiation of copulation. Whereas Darwin and others identified precopulatory adaptations associated with intrasexual competition (e.g., horns on beetles, status seeking in men), researchers studying sperm competition aim to identify postcopulatory adaptations. Thus, an alternative way of thinking about sexual selection is that there is not only competition between males for mates, but competition between males for fertilizations. Sperm competition is the inevitable consequence of males competing for fertilizations. If females mate in a way that concurrently places sperm from two or more males in their reproductive tracts, this generates selection pressures on males. If these selection pressures are recurrent throughout a species’ evolutionary history, males will evolve tactics to aid their sperm in outcompeting rivals’ sperm for fertilizations. These tactics may take the form of anatomical, physiological, and psychological adaptations. Although revolutionary for its time, the first definition of sperm competition, ‘‘the competition within a single female between the sperm of two or more males for the fertilization of the ova’’ (Parker, 1970, p. 527), does not capture the full spectrum of male anatomy, physiology, psychology, and behavior associated with sperm competition. SPERM COMPETITION AS AN ADAPTIVE PROBLEM IN HUMANS For species that practice social monogamy—the mating system in which males and females form long-term pair bonds but also pursue extra-pair copulations (i.e., ‘‘affairs’’)—it is the extrapair copulations by females that creates the primary context for sperm competition. A male whose female partner engages in an extra-pair copulation is at risk of cuckoldry—the unwitting investment of resources into genetically unrelated offspring—and its associated costs, which include loss of the time, effort, and resources the male spent attracting his partner and the misdirection of his current and future resources to a rival’s offspring. Consequently, in species with paternal investment in offspring, selection often favors the evolution of adaptations that decrease Address correspondence to Todd K. Shackelford, Florida Atlantic University, Department of Psychology, 2912 College Avenue, Davie, FL 33314; e-mail: [email protected]. CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE Volume 16—Number 1 47 Copyright r 2007 Association for Psychological Science the likelihood of being cuckolded. Anti-cuckoldry tactics fall into three categories: preventative tactics, designed to prevent female infidelity; sperm competition tactics, designed to minimize conception risk in the event of female infidelity; and differential paternal investment, designed to allocate paternal investment prudently in the event that female infidelity may have resulted in conception. The extent to which sperm competition occurred in ancestral human populations would have depended largely on rates of female sexual infidelity and cuckoldry. Current estimates of worldwide cuckoldry rates range from 1.7% to 29.8% (Anderson, 2006). Although current estimates of cuckoldry rates provide only a proxy of the occurrence of cuckoldry throughout human evolutionary history, even the most conservative estimates of these rates would have generated sufficient selection pressures on males to avoid the costs of cuckoldry. Moreover, the ubiquity and power of male sexual jealousy provides evidence of an evolutionary history of female infidelity and thus perhaps also of sperm competition. Male sexual jealousy can evolve only if female sexual infidelity was a recurrent feature of human evolutionary history, and female infidelity increases the likelihood that sperm from two or more men occupied concurrently the reproductive tract of a particular woman. This suggests that sexual selection, in the form of sperm competition, has been an important selection pressure during recent human evolution. If this is the case, then specific adaptations to sperm competition may have evolved. ADAPTATIONS TO SPERM COMPETITION IN HUMANS In this section, we discuss adaptations men may have evolved in response to an evolutionary history of sperm competition. We limit our discussion of these adaptations to testis size, ejaculate adjustment, semen displacement, sexual arousal, and forced inpair copulation, as these adaptations have been investigated more rigorously than others. Testis Size Across a range of animal species, males have relatively larger testes in species with more intense sperm competition. Because larger testes produce more sperm, a male with larger testes can better compete by inseminating a female with more sperm. Among the great apes, testes size varies predictably with the risk of sperm competition. In gorillas, female promiscuity and sperm competition are rare, and the gorilla’s testes are relatively small, making up just 0.03% of their body weight. Chimpanzees, in contrast, are highly promiscuous and, accordingly, males have relatively large testes, making up 0.30% of their body weight. The size of human testes falls between these two extremes at 0.08% of body weight, suggesting intermediate levels of female promiscuity and sperm competition in our evolutionary past (Shackelford & Goetz, 2006). Ejaculate Adjustment The number of sperm recruited into a given ejaculate is not constant. Although the physiology is not well understood, there is evidence that sperm number can be adjusted even moments before ejaculation (reviewed in Shackelford, Pound, & Goetz, 2005). A key hypothesis derived from sperm competition theory is that males will adjust the number of sperm they inseminate into a female as a function of the risk that their sperm will encounter competition from the sperm of other males. Baker and Bellis (1993) documented a negative relationship between the proportion of time a couple has spent together since their last copulation and the number of sperm ejaculated at the couple’s next copulation. As the proportion of time a couple spends together since their last copulation decreases, there is a predictable increase in the probability that the man’s partner has been inseminated by another male. Additional analyses documented that the proportion of time a couple spent together since their last copulation negatively predicts sperm number ejaculated at the couple’s next copulation, but not at the man’s next masturbation (Baker & Bellis, 1993). Inseminating into a female more sperm following a separation may function to outnumber or ‘‘flush out’’ sperm from rival men that may be present in the reproductive tract of the woman. Inspired by Baker and Bellis’s (1993) demonstration of male physiological adaptations to sperm competition, Shackelford et al. (2002) documented that human male psychology may include psychological adaptations to decrease the likelihood that a rival man’s sperm will fertilize a partner’s ovum. For example, men who spent a greater proportion of time apart from their partners since the couples’ last copulation—and, therefore, face a higher risk of sperm competition—report that their partners are more sexually attractive, have more interest in copulating with their partners, and believe that their partners are more interested in copulating with them, relative to men spent a lesser proportion of time apart from their partners. These effects were independent of relationship satisfaction, total time since last copulation, and total time spent apart, which rules out several alternative explanations (although other plausible alternative mechanisms remain to be evaluated). These perceptual changes may motivate men to copulate as soon as possible with their partners, thereby entering their sperm into competition with any rival sperm that may be present in their partners’ reproductive tracts. Semen Displacement Features of the penis may have evolved in response to the selective pressures of sperm competition. The penis of the damselfly is equipped with spines that can remove up to 99% of the sperm stored in a female, and the penis of the tree cricket is designed structurally to remove rival sperm prior to insemination of the male’s own ejaculate. Spines, ridges, and knobs on the penis of some waterfowl are positioned in a way to displace 48 Volume 16—Number 1 Sperm Competition