Product Code Database
Sexual swelling, sexual skin, or anogenital tumescence refers to localized engorgement of the anus and vulva region of some female 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 Human and Vervet monkey. 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 (the graded-signals hypothesis) combines several existing theories in the attempt to provide a more comprehensive account of sexual swellings.
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, and . 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, Gelada, Papio and Pan, and in most , Colobinae and .
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 group social systems, in which females mate promiscuously. (1976). 9780521212878, Cambridge University Press. ISBN 9780521212878 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. (1999). 9780511542466, Cambridge University Press. ISBN 9780511542466 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 , also exhibit exaggerated sexual swellings.Thornhill, R., & Gangestad, S. W. (2008). The evolutionary biology of human female sexuality. Oxford University Press.
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 , the state of maximum dorsality correlates with the period of maximum swelling.
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 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 Sexual conflict against them. Younger males have a slightly increased likelihood of conceptive mounting outside of peak swelling (e.g. early in the estrous cycle).
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 ( Papio cynocephalus) 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.
With the assumption that females require a certain number of copulations before they can conceive, this would suggest that they may achieve this number faster either by having a high number of ovulatory cycles between conceptions, or by appearing more attractive to males around the time of ovulation by having larger swellings. However, more obvious ovulation leads to more male coercion, which may have negative consequences, such as undesired consortship from a low-ranking male, or injury from forcible mating. Therefore, females will only accept this high level of coercion if the scramble competition in their community is high, and if the coercion will allow them to reach their required number of copulations in a short time. For example, eastern chimpanzees who have previously produced offspring tend to experience high within-group scramble, and so are driven towards having fewer ovulatory cycles between conception. As a result, they need to mate with a high number of males during each ovulatory period. They therefore need to appear more attractive during these periods, and so they develop larger sexual swellings.
Although Wrangham's model was justified by his observations, there has not been much other support for the hypothesis. Deschner and Boesch investigated the hypothesis directly by observing the same species and found that it was unable to support their results, and so proposed the social passport hypothesis as an alternative.
Under this hypothesis, young females who have safely integrated within the new community still benefit from sexual swellings. Specifically, young females are believed to require the support of the males acquired when integrating into the new group during conflicts with females of a higher social rank, or when protecting their infants from fights with the children of these higher-ranking females. Therefore, sexual swellings act as a social passport that eases female-female interactions.
Investigation into the social passport hypothesis has yielded contradictory results. Observations of common chimpanzees ( Pan troglodytes) in the Tai Forest, for instance, led to the discovery that sterile adolescent females or subordinate mothers exhibit swellings upon their emigration to new communities, suggesting that the swellings do indeed function to eliminate any social stress that could be directed at them during the emigration period. However, research on olive colobus ( Procolobus verus) residing in the same region showed females to emigrate without displaying sexual swellings. On the basis of this evidence, it has been suggested that the social passport hypothesis is not an appropriate explanation of the function of sexual swellings in this species.
The male services hypothesis is praised for its ability to account for the evidence that swellings do not always precisely indicate ovulation; the lack of precision is likely to extend the duration of mate guarding and consortship behaviours outlined by the hypothesis. Some of its predictions are not met, however. For instance, despite the benefits of a reduction in harassment from subordinate males when with dominant males, it has been observed that females do not always choose to mate with these stronger and more dominant mates.
The obvious-ovulation explanation of sexual swellings is consistent with the observation that ovulation often coincides with maximum swelling. Further support that males use swellings in the way set out by this hypothesis to assess the timing of ovulation comes from observations that in wild long-tailed macaques ( Macaca fascicularis): males are more aroused and find females more attractive at peak swelling. Others have been critical of this hypothesis, however. According to Stallman and Froehlich's assessment, the hypothesis predicts monandry (i.e. that females will have only one mating partner), which runs counter to observations of species such as Barbary macaques ( Macaca sylvanus), which have exaggerated sexual swellings, yet have been seen to be promiscuous and polyandrous (i.e. mating with multiple males) in their mating behaviours.
Support for this hypothesis argues that it accounts for some of the correlates and characteristics of sexual swellings, such as the proximity of peak swelling to ovulation, and increased male-male competition over females at peak swelling. The best-male hypothesis has been criticised, however, for its inability to account for the exaggerated nature of these swellings. Specifically, Pagel argued smaller swellings would be sufficient to incite competition between males since this behaviour was calculated to be an evolutionarily stable strategy. Others have criticised the assumption that the male which is successful in competition for swollen females (i.e. the most dominant) would also be the females own choice of partner, as it has been observed that some females choose to mate with subordinate males.
To successfully ensure paternal confusion, Hrdy predicted that ovulation must be randomly distributed across the term where the sexual swelling is of maximum tumescence. This would ensure that males were unable to use the swelling as a signal of female fertility. One example of this stems from research into sooty mangabey ( Cercocebus atys); the females of this species have been found to produce sexual swellings both when they are fertile and when they are with child. Additionally, sexual swellings are only observed during the most fertile period of a female's menstrual cycle in 26-35 species of anthropoid primates, in contrast to Hrdy's prediction.
Sexual conflict is considered, within this hypothesis, to be a key factor in the development of exaggerated sexual swellings. As male reproductive strategies of coercion (including infanticide and prolonged mate-guarding) may be costly to females, it has been necessary for females to resist these through developing features or counter-strategies that will protect them whilst still allowing for successful reproduction. This can be explained through the combination of a number of previously mentioned hypotheses; most notably obvious-ovulation, best-male, and many males.
In terms of obvious-ovulation, the swelling of the perineal skin has been likened to a Bell Curve that would represent that probability that the female would ovulate, with larger swellings suggesting that ovulation is more likely to occur. As such, females are more likely to attract the attention of dominant, or "better", males when their swelling size peaks, and it has been shown that dominant males tend to only mate-guard at this peak swelling point, thus including the best-males hypothesis. This mate-guarding is costly to the male, and so they tend only to monopolise any single female for the most likely period of ovulation; once her swellings start to shrink, the male will move onto a female whose swellings are still growing to reach their peak. In these periods before and after the peak, females still continue to mate with lower-ranking males, as their probability of ovulation is not so high, but conception is still possible. This then serves to confuse the paternity of the offspring amongst the males, linking to the many-males hypothesis, and also resulting in reduced infanticide by the males within the species. Therefore, the protective role of the swellings against male coercion serve, in some ways, to manipulate male behaviour into benefiting the female, and enhancing the female's chances at successful reproduction.
As one of the more recent hypotheses, the graded-signals hypothesis still has limited research supporting it as the evolutionary function of sexual swellings. However, the growing literature base is supportive of the hypothesis; if not as the sole reason behind the evolution of the swellings, then perhaps in conjunction with the reliable indicator hypothesis.
For such a signalling system to be a reliable indicator of quality, it must fulfil two criteria: that the trait is costly to produce, and that mating effort is costly for the males in the group. In regards to sexual swellings, both of these ring true. In terms of costliness, swellings affect a female's weight and centre of gravity, affecting their ease when travelling. The skin itself increases vulnerability to predators due to its conspicuousness, as well as to infection. Additionally, the increased attention from males also puts females at a risk of injury through male aggression. In terms of the cost to males, mate guarding has been found to significantly reduce foraging in male baboons, therefore reducing their available food. Additionally, males expend effort in both grooming and consorting the female with whom they are mating, as well as warding off other males; the more attractive the female is, the greater the male-male competition, therefore increasing the risk to the male, as fights between baboons are potentially lethal.
Although Pagel performed a field experiment which found support for all predictions of the hypothesis through the observation of ( Papio anubis), its methodology has since been criticised, and subsequent research has failed to find empirical evidence that sexual swellings reliably indicate female quality in this, and other, species (e.g. , , and ). For example, one of the main predictions is that higher quality, and therefore most fertile, females should consistently display the largest swellings. However, the largest swellings often occur in the least fertile females, or those least likely to raise surviving offspring; adolescents, those that have never borne offspring, and those that have had several ovulation cycles without conceiving.
Despite the lack of empirical evidence for this hypothesis being the sole evolutionary function for exaggerated sexual swelling, it has been suggested that the reliable indicator hypothesis may work together with the graded-signals hypothesis. This suggestion is based on evidence that swelling size advertises the level of fertility, and therefore reproductive quality, between one female's ovulation cycles, rather than between the overall quality of each female. Therefore, males may initially use swelling size as a cue to identify which females are close to ovulation (as predicted by graded-signals), before considering each females' swelling size as an indicator of their quality, and then choosing the female with the larger swelling (as predicted by reliable indicator). This would also account for the variable patterns in swelling size fluctuation across species and populations.
|
|
