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

Journal of Sex Research, Feb, 2004 by Kim Wallen, Julia L. Zehr

   With respect to sexuality, I have often speculated on it, and have
   always concluded that we are too ignorant to speculate: no
   physiologist can conjecture why the two elements go to form a new
   being, and, more than that, why nature strives at uniting the two
   elements from two individuals. (Darwin, 1861, in Darwin, 1903)

In the preceding quote, Darwin's reference to "sexuality" was in the sense of sexual reproduction. We are, however, similarly ignorant about the behavior that accompanies sexual reproduction, the now conventional use of the term sexuality. What are the causes for engaging in sexual behavior? Why does sexual behavior vary across development and across species? What brings two individuals together so that their gametes can combine? We have partial answers to some of these questions, while answers for others remain elusive. However much of what is understood reflects the reality that sex is expensive, dangerous, and time consuming. The evolution of sex and the selective advantage it conveys are matters of controversy, with explanations ranging from the advantages of recombination (Charlesworth, 2002) to rapid adaptation in a changing environment (Colegrave, 2002). The only thing that can be stated with certainty is that the evolution of sex remains a puzzle, while its pervasiveness argues for a strong, as yet unidentified selective advantage to sexually reproducing species. Beyond the question of sex itself as a reproductive mechanism lies why different forms of sexual reproduction have evolved, from sequential deposition of gametes by males and females separated in time and place to internal fertilization requiring sexual intercourse and gestation. This variation suggests that sexual reproduction carries significant costs producing substantial selective pressure to create diverse solutions to the problem of sex. This paper focuses primarily on the implications and consequences of sexual reproduction for females in species relying upon internal fertilization and gestation for their reproductive output. More specifically, we discuss why sex may have evolved and attempt to answer the proximal questions of why sexual behavior occurs, what mechanisms modulate sexual behavior, and what mechanisms ensure the occurrence of sexual behavior when reproduction is possible.

THE RISK OF SEX

That sex is dangerous in internally fertilizing species is without doubt. By its nature, sexual intercourse requires a close and cooperative association between male and female that is not present in any other social behavior. Physical injury is always possible, especially when size and strength disparities exist between the sexes, and sexual intercourse, which requires penetration of one body by part of another, carries its own special risk of injury. Sexual intercourse provides the context for sexual aggression and sexual coercion, which has been found in a wide variety of mammals ranging from humans to water voles (Smuts & Smuts, 1993). In elephant seals, for example, researchers found that 1 in 1,000 adult female elephant seals was killed during mating (Le Boeuf & Mesnick, 1991), illustrating the cost of sexual reproduction. Sexual intercourse itself can injure the genitalia. Both penile fracture (Eke, 2002) and vaginal tearing, often requiring suturing (Anate, 1989; Dao, Diouf, Bambara, Bah, & Diadhiou, 1995) have been reported. However, the injuries need not be so severe. One study found that 61% of women had vaginal microtrauma following sexual intercourse, whereas only 11% of these women had similar trauma when they had not had intercourse during at least 3 days prior to vaginal inspection (Norvell, Benrubi, & Thompson, 1984). Together such findings illustrate the increased risk of death and injury associated with sexual reproduction.

The potential physical risk of sex puts a premium on social skills and social cognition that allow sex to occur with minimal physical risk. However, even the best of social circumstances do not eliminate the risk that sex places on both partners, as successful sexual intercourse is also conducive to the transmission and growth of pathogens that can kill or maim their hosts. Risk of infection has likely been a strong selective force in the evolution of sex. More than 200 sexually transmitted pathogens have been reported in animals covering a wide phylogenetic range (Lockhart, Thrall, & Antonovics, 1996). It has been suggested that menstruation evolved to protect against sperm-borne pathogens (Profet, 1993; Sobo, 1994). While it seems more likely that menstruation evolved in association with gestation rather than as a pathogen-protection mechanism (Finn, 1998; Strassmann, 1996), sexual intercourse as an avenue for disease transmission is undeniable and likely influenced the evolution of reproductive behavior.

Gestation adds additional risks to those already associated with internal fertilization. Gestation increases maternal energetic demands thereby, threatening the mother's survival; decreases mobility, thus increasing predation risk; and requires specific adaptations for birth. While birth can be relatively easy in some species, such as fish and reptiles, in mammals the increased size of offspring markedly increases maternal mortality. In one extreme case, the spotted hyena, birth requires splitting of the female's pseudo penis to provide a birth canal (Frank, 1997). In humans, pregnancy and childbirth presents significant risk, with the magnitude of the risk varying across cultures. Female mortality associated with child-bearing in Sweden was 7.4 deaths per 100,000 live births (Kwast, Rochat, & Kidane-Mariam, 1986) from 1980 to 1988. In contrast, maternal death in Ethiopia in 1983 was 566 deaths per 100,000 live births (Kwast et al., 1986). A direct comparison of mortality rates between pregnant and non pregnant women in rural Malawi, found that pregnancy increased female mortality by 29 per 100,000 women (McDermott et al., 1996). Although generating accurate population comparisons is difficult, there is little doubt that pregnancy significantly increases maternal mortality. These risks, however, are possibly offset by the increased nutrition and protection directed toward the developing fetus, which in turn increases reproductive success. Again, as in the case of internal fertilization, gestation must offer a substantial selective advantage to offset the increased maternal mortality and debilitation that it produces.