Sexual swelling

Sexual swelling, sexual skin, or anogenital tumescence refers to localized engorgement of the anus and vulva region of some female primates that vary in size over the course of the menstrual cycle. Thought to be an honest signal of fertility, male primates are attracted to these swellings; preferring, and competing for, females with the largest swellings. Sexual swelling is widespread among primates but completely absent in humans and vervet monkeys. Females of these species exhibit concealed ovulation.
Though heavily investigated, the ultimate function of sexual swellings remains unknown. Over the last 50 years, eight principal explanations have been proposed, each claiming to account for the function of exaggerated swellings. Alone, however, no single hypothesis is believed to account for the function of sexual swellings; a combination of these theories may be more appropriate. In line with this ideal, the most recent account regarding the function of sexual swellings combines several existing theories in the attempt to provide a more comprehensive account of sexual swellings.

Characteristics

Physical characteristics and correlates

Sexual swellings are concentrations of tumescent tissue, cyclically appearing on the genitalia and adjacent posterior regions of female primates. The exact reproductive purpose of sexual swellings is not fully understood, though the erogenous sensitivity of this tissue is known to motivate females to pursue sexual contact with males. The position of swellings can heavily influence the location of male focus during courtship, and of eventual penetrance. Among chimpanzees, bonobos, baboons, and many Old World monkey species, it is common for swellings to concentrate in the perineal, perianal, and coccygeal regions, rather than more ventrally in the area of the vulva. Dorsal swelling positions can therefore correlate with frequent non-conceptive, penetrant mounting, thus enhancing high volume/low efficiency female mating strategies, which guard against incidental impregnation by opportunistic low-tier males during peak fertility.
Swellings can be categorized into two groups: small and exaggerated. Small swellings are characterised by a moderate size and pinkness of the anogenital tissue, and can be found in Old World monkeys, New World monkeys, prosimians and gibbons. In contrast, exaggerated swellings are larger in size, and their prevalence is mainly restricted to Old World primate species. For instance, they occur in all species of Cercocebus, Mandrillus, Theropithecus, Papio and Pan, and in most macaques, colobines and guenons.
Researchers have attempted to determine the characteristics of the primate species displaying these exaggerated swellings. It has been identified that species which exhibit exaggerated sexual swellings predominantly live in multi-male social systems, in which females mate promiscuously. Species with such swellings have twice as many males per group than those without. Furthermore, whilst 71% of Old World primate species living in multi-male groups show exaggerated swellings, no females living within single-male groups do. In some instances, however, sexual swellings can be seen in primate societies with alternative mating systems; for example, female langur monkeys exhibit swellings but live within polygamous single-male groups.
Primates with exaggerated sexual swellings also demonstrate non-seasonal breeding patterns, longer mating periods and longer ovulation cycles. Specifically, of the 23 species which are both non-seasonal breeders and live in multi-male societies, 91% have sexual swellings. Nonetheless, nonseasonal reproductive environments are not a necessary precursor for the selection of sexual swellings. Indeed, females who are seasonal breeders, such as the female Barbary macaques, also exhibit exaggerated sexual swellings.

Changes across the menstrual cycle

Exaggerated sexual swellings vary both in size and focal location throughout the female's cycle, beginning after menstruation. For example, research on baboons showed that after 14 days of gradual increase, swellings peaked for 2 days before reducing. Female chimpanzees exhibit a shift in swelling prominente. These cyclic changes in appearance of the sexual skin reflect the changes of ovarian hormones during the female menstrual cycle. Specifically, the increase in sexual swelling size during the follicular phase is correlated with increased estrogen levels, and the decrease in swelling size during the luteal phase is associated with rising progesterone levels. It has been shown in ovariectomized chimpanzees that swelling can be induced by estrogen and inhibited by progesterone. As a result, the peak size of the swellings often coincides with the highest potential of ovulation, although this is not a perfect association. For example, research on West African chimpanzees showed that higher probabilities of ovulation tended to occur within 7 to 9 days of the onset of maximum swelling of sexual skin. Additionally, a study into wild white-handed gibbons showed that maximum swelling size and ovulation overlapped closely in 80% of menstrual cycles.
The size of sexual swellings not only varies within each cycle, but also across female cycles and across species. Specifically, the maximal swelling size increases from cycle to cycle for individual female chimpanzees and baboons. Additionally, the duration of maximal sexual swellings size varies considerably between species. Baboons for instance, have a maximal swelling lasting approximately 15.1 days, whilst the duration of maximal swelling is 10.9 days in chimpanzees.
Like size, location also varies considerably across the cycle. For instance, in chimpanzees, the state of maximum dorsality correlates with the period of maximum swelling.

Male responses to sexual swellings

Male primates are highly attracted to females when their sexual swellings are largest, and demonstrate preferential mating during periods of maximal swelling. Males tend to compete more for females whose swellings are at their maximum point. Male–male competition peaks, and males attempting to mate with the females with the largest swellings receive increased levels of aggression from other males as a result. Observations of chimpanzees have revealed that the presence of at least one female who was maximally swollen prompted higher levels of aggression between males in a group, as well as increased levels of sexual behaviour.
In general, males respond to female sexual swellings as though they provide indications of female fertility, using these swellings to determine their level of investment and effort in courting females. In male baboons, mating effort is determined by the size of the female's swellings, which, in turn, impacts levels of male-male aggression, competition and fighting behaviours, as well as how much time is invested in grooming and courting the female. Peak swelling also correlates with higher levels of mate guarding behaviour, with males preferring to guard those females whose swellings are close to or at maximal swelling, as well as performing more inspections of their anogenital areas.
The greater access to the most swollen females is usually granted to and won by the most dominant males in the group. Those further down the hierarchy tend to only be able to gain access and mate with females outside of these periods of peak swelling when the competition for them is reduced and the attention of more dominant males has shifted to the more swollen females in the group. In baboons, the more mature and dominant males mate most repetitively with the most receptive females at peak swelling. Young males get access to mate, though much less frequently, and only within the confines of female baboon mating strategy, which advantages non-conceptive mounting as a defense against them. Younger males have a slightly increased likelihood of conceptive mounting outside of peak swelling.

Function

Though much is understood about the physical characteristics of sexual swellings, their exact functional significance remains controversial. The role of sexual selection in the evolution of these swellings features in many hypotheses, and has, since Darwin, been assumed to play a significant role. Hypothesised functions of sexual swellings often focus on swellings in terms of female mating strategies. These range from advertising fertility and quality, maximising potential mates to confuse paternity of offspring, to aiding in a female's assessment of the best possible mating partners, and even assuring paternity certainty, and all aim to account for aspects of exaggerated sexual swellings. This section covers the range of hypotheses that provide explanations of proposed functions for these swellings.

Sensory exploitation hypothesis

An altered version of Holland and Rice's chase-away model is cited to explain the function of sexual swellings. The chase-away model is governed by the idea of "sensory exploitation", in which traits evolve to greatly stimulate the perceivers' sensory system. As a result, these traits serve to manipulate a perceiver's behaviour in favour of the signaller. In the specific case of sexual swellings, it is a male's inherent preference for large swellings as a signal of fertility is exploited to combat male resistance to mate Therefore, small sexual swellings are thought to have become exaggerated as a form of antagonistic coevolution.
The association found between female fertility and sexual swelling size in several species of macaque offers support for this hypothesis. Specifically, females of low fertility, such as adolescents, exhibited substantially larger swellings than adults of a higher fertility level. Research remains fairly consistent across animal species; female yellow baboons who struggle to conceive are, on average, those that display the most prominent sexual swellings. In contrast, some have been critical of the sensory exploitation theory; they uphold the belief that, if female sexual swellings were not honest signals of female fertility, males would have evolved to identify differences in female quality or to have equal preference over females with different swelling sizes.