Female Mate Choice as a Significant Selective Force
Writer’s comment: As an anthropology student, I listened to several professors explain how females of many animal species influence the direction of evolutionary change through their choices of particular mates. Often cited was a famous study showing that certain female birds prefer mates with ridiculously long tail feathers—even if the feathers are glued on researchers! However, each time this favorite topic was addressed, I was disappointed to hear that female choice among my nonhuman primate cousins was considered an insignificant evolutionary force. I always wondered how this could be. I thought it inconceivable that females had no interest in actively choosing a suitable mate. Why should females bear less selective impact than males? The feminist in me set out, in English 104E (Scientific Writing), to prove the experts wrong, and I was pleasantly surprised at the overwhelming amount of evidence that agreed with me.
- Lisa Mueller
Instructor’s comment: Lisa Mueller wrote this review of literature for my English 104E: Scientific Writing course. The assignment was to write a review paper that would bring readers up to date on a scientific topic or problem of critical importance, synthesizing material from a number of journal articles. In her review, Lisa very clearly lays out the line of research on the topic of “female mate choice” in nonhuman primates, letting readers know what is known on this topic, what is not known, and what paths future research will likely take. Her paper is a well-organized, clear, and articulate review on a topic that will interest a wide spectrum of readers.
- Linda Bates, English Department
Darwin argued that certain characteristics could not have evolved by natural selection (cited in Harcourt, 1995). These traits, he proposed, do not perpetuate the survival of the individual, but rather they increase the reproductive success of the individual, and hence, the traits must have evolved by some other process. Darwin called the process sexual selectionand explained that it consists of two separate aspects: male-male competition and female mate choice. Male-male competition for females, or intrasexual competition, acts as a significant selective force because the stronger, larger male with more fierce tactics and weapons almost always wins the fight and thus wins the mating. Female mate choice, formally known as intersexual selection, is a strong evolutionary force in many species because it is the female who decides which males will mate, and hence, contribute genes to future generations.
Female choice has been considered a less important evolutionary force in nonhuman primates by those who insist that the female does not actively choose her mate, but rather, she merely submits to matings with the winner. The purpose of this review is to present recent research indicating that female, nonhuman primates are indeed exerting some influence on which male genes are let into the pool. I will present results of studies of the last decade showing that these females are choosing the fathers of their offspring by directly initiating copulations, refusing matings with unfit or unattractive males, and performing pre-copulatory penis inspections. I will also discuss anti-sperm responses in the female reproductive tract that female primates have obtained through their mammalian heritage. These responses select against undesired spermatozoa. Finally, I will provide new evidence that in at least one nonhuman primate species, female choice has a greater influence on male reproductive success than male-male competition.
It is surprising that female mate choice has developed secondary importance to intrasexual competition despite overwhelming evidence of female initiation of sex in nearly every primate species studied (Smuts, 1987). Females in the majority of species display their interest in a particular male by presenting their hindquarters to him just prior to copulation (Hrdy & Whitten, 1987). According to one research group, several species have evolved even more elaborate means of informing males of their mating prospects (Hrdy & Whitten, 1987). Ruffed lemurs, Varecia variegata,slap desired males, rub their bodies against them, and then quickly dart away. Callithrix jacchus,the common marmosets, flick their tongues, arch their backs, crouch, and piloerect their fur. Grabbing and jerking the head of an attractive male is the preferred technique of Barbary macaques, while Patas monkeys, Erythrocebus patas,blow into their cheek pouches, drool, and hold their tails up in a curled position. Female orangutans touch their mouths to the genitals of chosen mates while hanging from above (Hrdy & Whitten, 1987).
Smuts (1987) suggests that in some instances, solicitation of sex by female primates is subtle and is often unnoticed by researchers who incorrectly assumethat only males influence the likelihood of copulation. One study of captive rhesus macaques revealed that males were successful at copulating with a female only if she previously glanced at him and maintained a particular posture (Smuts, 1987). However, because these gestures allowed the macaques to communicate with one another from relatively far distances, observers overlooked the gestures entirely and wrongly suspected that females were receptive to any males who attempted to mount them (Smuts, 1987).
Females of virtually all primate species have also been witnessed refusing the mating attempts of males (Smuts, 1987). Often an uninterested female will walk away from a mounting male, or she may sit down, preventing penetration (Smuts, 1987; Nishida, 1997). Aggression may even be used by females to discourage unwanted copulations in some primate species: bushbabies (Galagospp.), fat-tailed dwarf lemurs (Cheirogaleus medius),vervets (Cercopithecus aethiops),talapoins (Miopithecus spp.),and gelada baboons (Theropithecus gelada)(Smuts, 1987). Rape has been observed in just one of the approximate two hundred species of primates (Smuts, 1987). The fact that only orangutan males use such force to acquire matings is a clear indication that the female’s choice is significant in the vast majority of nonhuman primates (Smuts, 1987).
Pre-copulatory Penis Inspections
In a recent study detailing mating behaviors of the chimpanzees of the Mahale Mountains National Park in Tanzania, Toshisada Nishida (1997) was the first to report that female chimps are occasionally observed performing a pre-copulatory penis inspection, or “erection check,” to determine the condition of potential mates. Nishida (1997) describes the phenomenon:
An estrous female . . . approached a sitting male, stood on all fours, and peered between his thighs, apparently checking whether his penis was erect or not. If the penis was not erect, she soon left him; if it was erect, she would assume a presentation posture and even push herself between his thighs. Then, if the male did not respond, she would show frustration such as thumping or branching. One chimp named Chausiku was even seen attempting to stimulate the flaccid penis of a desired partner following an erection check (Nishida, 1997). Although similar penis inspection behaviors have been described in dusky titi monkeys (Hrdy & Whitten, 1987), the behaviors likely communicated a female titi’s readiness to mate, rather than her choice of mates because dusky titi monkeys are a strictly monogamous species. Nishida, therefore, provides the first evidence that such inspection serves as a vehicle for female choice.
Anti-sperm Responses in the Female Reproductive Tract
Females may even continue to exercise their choice after copulation. Myriad obstacles and anti-sperm responses in the female reproductive tract allow just a few of the millions of sperm in the mammalian male’s ejaculate to reach the female’s egg and attempt fertilization. Birkhead, Moller, and Sutherland (1993) propose that the hostile environment of the vagina may have originally evolved to protect the female against bacterial and viral infection, or to prevent polyspermic fertilization, but the mammalian female has taken advantage of the harsh environment to use it as a means of selecting which spermatozoon fertilizes her egg.
Evidence that the female is indeed rejecting sperm is strong. Some mammals, including the woolly spider monkeys, Brachytelesspp., have frequently been observed actively expelling sperm from the vagina in the hours following insemination (Birkhead et al., 1993). Moreover, mammalian females have numerous barriers to sperm in their reproductive tracts. The first is the cervix, which acts as a physical barrier that many sperm are unable to penetrate (Birkhead et al., 1993). The chemical composition of the mucus surrounding the cervix is also highly unfavorable to sperm, and in some cases a leukocyte attack specific to sperm results in the phagocytosis and subsequent death of thousands of spermatozoa in the vicinity of the cervix (Birkhead et al., 1993; Birkhead & Moller, 1993). Finally, anti-sperm antibodies in the cervical mucus of many mammals attack sperm and block them from entering the cervix (Birkhead et al., 1993).
However, evidence that mammalian females, including primates, are rejecting sperm is not necessarily evidence that they are actively selecting which sperm will fertilize their ova. Nevertheless, Birkhead et al. (1993) argue that in making it extremely difficult for sperm to make their way to the egg, females are selecting spermatozoa of exceptional quality to be passed on to their male offspring. By inheriting sperm that can withstand the many obstacles and anti-sperm responses of the female reproductive tract, these females’ sons will be more successful in fertilizing the ova of their future mates (Birkhead et al., 1993). Furthermore, because a female’s reproductive success depends not only on her ability to produce offspring, but also on her offspring’s ability to produce offspring, it is in her reproductive interest to select superior sperm for her sons.
Female Choice as a Stronger Selective Force than Male Competition
In a landmark study of a captive population of Japanese macaques, a cross-continental team of researchers found that female mate choice is a stronger selective force than male-male competition (Soltis et al., 1997b). Using dominance rank as a measure of male-male competition and attractivityrank as a measure of female mate choice, Soltis et al.(1997b) discovered that a male’s reproductive success is better predicted by his attractiveness to females.
The researchers assigned dominance ranks to the eight adult male macaques involved in the study, based on the outcomes of their dyadic interactions with one another (Soltis et al., 1997b). A linear dominance hierarchy was inferred because every encounter between a given dyad resulted in the submission of the same individual, as evidenced by grimacing, cowering, retreating, being supplanted by the opponent, and being the object of overt aggression (Soltis et al., 1997b). Hence, there was no ambiguity regarding an individual male’s position in the hierarchy (Soltis et al., 1997b). Each male was then assessed for his attractiveness to each of the thirteen adult females, based on the females’ maintenance of proximity to him. This attractivity rank was determined by subtracting the number of occasions on which a given female retreated from a given male in close proximity (defined as within 1 m) from the number of times the given female approached the male within 1 m (Soltis et al., 1997a).
The females subsequently came into estrus, and multiple matings were observed (Soltis et al., 1997a). Infants were born to twelve focal females and two females who were not originally involved in the study (Soltis et al., 1997b). DNA was collected from each infant, and microsatellite alleles were compared to those of the mother and each of the eight possible fathers (Soltis et al., 1997b). Definite paternity was determined for thirteen of the fourteen infants (Soltis et al., 1997b).
Through careful statistical analysis, Soltis et al. (1997b) revealed that only attractivity rank accurately predicted male reproductive success. A male’s position within the dominance hierarchy had no influence on whether or not he fathered an infant that breeding season (Soltis et al., 1997b). Thus, in at least one population of Japanese macaques, female mate choice is not only a significant selective force, but it is a stronger selective force than male-male competition.
Evidence substantiating the significance of female mate choice in sexual selection in nonhuman primates is overwhelming. Females in nearly every primate species initiate sex, often through quite elaborate, but subtle gestures that have been repeatedly overlooked by researchers. Moreover, females of virtually all primate species refuse matings with unfit or unattractive males. The fact that rape occurs only in orangutans clearly indicates that the female’s choice is significant in the vast majority of species.
Recent research describes females’ pre-copulatory inspection of their potential partners’ penises and suggests that such inspection serves as an instrument of mate selection for females of at least one primate species. Furthermore, Birkhead et al.(1993) argue that the multiple obstacles and anti-sperm responses of the mammalian female’s reproductive tract act as a means of selecting which spermatozoon will fertilize her egg. Most importantly, Soltis et al.(1997b) have shown that it may be a male’s attractiveness to females, and not his ability to intimidate and fight off other males, that actually determines his reproductive success. Thus, female mate choice is not only a significant aspect of sexual selection, but in some cases it may be more influential than male-male competition.
Future research is necessary to further elucidate the extent to which female mate choice is shaping primate societies. Currently, the work of Soltis et al.(1997a; 1997b) is the only known study to actually measure the force of intersexual versus intrasexual selection in a primate population. The replication of research of this caliber is essential if we are to truly understand the selective forces acting on our primate cousins. I speculate that such research will continue to shatter the prevailing notion that female mate choice is an insignificant selective force in nonhuman primates.
Birkhead T.R. and A.P. Moller. 1993. Female control of paternity. Trends in Ecol. and Evol. 8:100-104.
Birkhead, T.R., A.P. Moller, and W.J. Sutherland. 1993. Why do females make it so difficult for males to fertilize their eggs? J. Theor. Biol. 161:51-60.
Harcourt, A.H. 1995. Sexual selection and sperm competition in primates: What are male genitalia good for? Evol. Anthropol. 4:121-129.
Hrdy, S.B. and P.L. Whitten. 1987. Patterning of sexual activity. In Smuts, B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, and T.T. Struhsaker (Eds.), Primate Societies (pp. 370-384). Chicago, IL: University of Chicago Press.
Nishida, T. 1997. Sexual behavior of adult male chimpanzees of the Mahale Mountains National Park, Tanzania. Primates 38:370-398.
Smuts, B.B. 1987. Sexual competition and mate choice. In Smuts, B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker (Eds.), Primate Societies (pp. 385-399). Chicago, IL: University of Chicago Press.
Soltis, J., F. Mitsunaga, K. Shimizu, Y. Yanagihara, and M. Nozaki. 1997a. Sexual selection in Japanese macaques I: Female mate choice or male sexual coercion? Anim. Behav. 54:725-736.
Soltis, J., F. Mitsunaga, K. Shimizu, M. Nozaki, Y. Yanagihara, X. Domingo-Roura, and O. Takenaka. 1997b. Sexual selection in Japanese macaques II: Female mate choice and male-male competition. Anim. Behav. 54:737-746.