Hormones and history: the evolution and development of primate female sexuality

Abstract

Sexual behavior is required for reproduction in internally fertilizing species but poses significant social and physical risks. Females in many nonprimate species have evolved physical and behavioral mechanisms restricting sexual behavior to when females are fertile. The same hormones producing female fertility also control these mechanisms, assuring that sex only occurs when reproduction is possible. In contrast to nonprimate mammals, hormones do not regulate the capacity to engage in sex in female anthropoid primates, uncoupling fertility and the physical capacity to mate. Instead, in primates, sexual motivation has become the primary coordinator between sexual behavior and fertility. This dependence upon psychological mechanisms to coordinate physiology with behavior is possibly unique to primates, including humans, and allows a variety of nonphysiological influences, particularly social context, to regulate sexual behavior. The independence between hormonal state and sexual behavior allows sex to be used for social purposes. This complex regulation of primate sexuality develops during adolescence, where female monkeys show both hormonally influenced sexual motivation and socially modulated sexual behavior. We present findings from rhesus monkeys illustrating how social context and hormonal state interact to modulate adolescent and adult sexuality. It is argued that this flexibility in sexual behavior, combined with a tight regulation of sexual motivational systems by reproductive hormones, allows sexual behavior to be used for nonreproductive purposes while still assuring its occurrence during periods of female fertility. The evolutionary pressures that produced such flexibility in sexual behavior remain puzzling, but may reflect the importance of sexuality to primate social attraction and cohesion.

Figure 1

Female sexual initiation during ovulatory (A) and anovulatory (B) menstrual cycles in individual early adolescent females, illustrating that both social context and circulating hormones affect the expression of adolescent sexual behavior. Two of three females who ovulated around 2.5 years of age showed periovulatory female sexual initiation. The highest ranked females showed more interest in males, during both ovulatory and nonovulatory cycles, than did the middle and tower ranked females.

Figure 2

Female sexual initiation in high, middle, and low ranked females during late adolescence, illustrating that high ranked females had higher levels of sexual initiation and a less tight coupling of behavior with the periovulatory period of their ovarian cycles than did middle and low ranked females.

Figure 3

Female sexual initiation in early and late adolescence in three females who first ovuluted during early adolescence, illustrating that the frequency of sexual initiation increased from early to late adolescence.