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Concealed ovulation or hidden estrus is the lack of distinctive signaling that the adult female of a species is "in heat". These signals may include swelling and redness of the genitalia in baboons and bonobos Pan paniscus, pheromone release in the feline family, etc. By comparison, the females of humans and a few other species have few external signs of fecundity, making it difficult to tell, by means of external signs only, whether or not a female is near ovulation.

Concealed ovulation in women

While women can be taught to recognize their own level of fertility (fertility awareness), whether men can detect fertility in women is highly debated. Several small studies have found that fertile women (compared to women in infertile portions of the menstrual cycle or on hormonal contraception) appear more attractive. It has also been suggested that a woman's voice may become more attractive to males during this time. Two small studies of monogamous couples found that women initiated sex significantly more frequently when fertile, but male-initiated sex occurred at a constant rate in all phases of the menstrual cycle.

Analyses of data provided by the post-1998 U.S. Demographic and Health Surveys found no variation in the occurrence of coitus in the menstrual phases except during menses. These findings of differences in female-initiated sex versus male-initiated sex are likely caused by the female’s awareness of her ovulation cycle (because of hormone changes) but the male’s inability to detect ovulation because of its being “hidden.”

In 2008, researchers announced the discovery of hormones related to ovulation in human semen. They theorized that follicle stimulating hormone, luteinising hormone, and estradiol may encourage ovulation in women exposed to semen. These hormones are not found in the semen of chimpanzees, suggesting that this phenomenon may be a male counter-strategy to concealed ovulation in human females. Other researchers are skeptical that the low levels of hormones found in semen could have any effect on ovulation. One group of authors has theorized that concealed ovulation and menstruation were key factors in the development of symbolic culture in early human society.

Evolutionary hypotheses

There are many questions concerning concealed ovulation, specifically why and when it occurred. Natural selection retains traits that increase the fitness of the individual, meaning that the traits of those individuals who reproduce the most viable offspring will be selected for and maintained in the species. The following hypotheses thus try to examine the adaptive advantages for the evolution of concealed ovulation in human females. It could be that the lack of signaling in some species is a retained ancestral trait, not something that existed previously and later disappeared. If signaling is supposed to have existed and was lost, then it could have been merely due to reduced adaptive importance and lessened selection, or due to direct adaptive advantages for the concealment of ovulation. Yet another possibility, specifically for humans, is that while highly specific signaling of the ovulation is absent, the female form evolved to mimic permanent signaling of fertility. There are several hypotheses that aim toward answering these questions. It may be possible for elements from multiple hypotheses to be true.

Paternal Investment Hypothesis

This hypothesis is strongly supported by many evolutionary biologists. Several hypotheses regarding human evolution integrate the idea that human females increasingly required supplemental paternal investment in their offspring. The shared reliance on this idea across several hypotheses concerning human evolution increases its significance in terms of this specific phenomenon.

This hypothesis suggests that human females concealed ovulation in order to obtain male aid in rearing offspring. Schroder summarizes this hypothesis outlined in Alexander and Noonan’s 1979 paper. If human females no longer signaled the time of ovulation, males would be unable to detect the exact period in which they were fecund. This led to a change in their mating strategy; rather than seeking multiple female partners and mating with them hoping that they were fecund during that period, males instead chose to mate with a particular female multiple times throughout her menstrual cycle. A mating would be successful in resulting in conception when it occurred during ovulation, and thus, frequent matings, necessitated by the effects of concealed ovulation, would be most successful.

Continuous female sexual receptivity suggests that human sexuality is not solely defined by reproduction; a large part of it revolves around conjugal love and communication between partners. Copulations between partners while the female is pregnant or in the infertile period of her menstrual cycle do not achieve the base purpose of sex – conception – but do strengthen the bond between these partners. Therefore, the increased copulations because of concealed ovulation are thought to have played a role in fostering pair bonds in humans.

The pair bond would be very advantageous to the reproductive fitness of both partners throughout the period of pregnancy, lactation, and rearing of offspring. Pregnancy and lactation require vast amounts of energy on the part of the female, necessitating a large amount of energy intake in the form of food. However, during these periods, the female’s foraging ability would be greatly hindered because of constraints placed upon her by the pregnancy itself or the amount of time tending to or minding the offspring. Supplemental male investment in the mother and her offspring is advantageous to all parties. While the male is supplementing the female’s limited foraging intakes, she can devote the necessary time to the care of her offspring. The offspring benefits from the supplemental investment, in the form of food and defense from the father, and receives the full attention and resources of the mother. Through this shared parental investment, both male and female would increase their offspring’s chances for survival, thereby increasing their reproductive fitness. This increased reproductive fitness is the key to natural selection favoring the establishment of pair bonds in humans and since pair bonds are thought to have been strengthened by concealed ovulation, this must have been under selective pressure.

Reduced Infanticide Hypothesis

This hypothesis suggests that the adaptive advantage for females that had hidden estrous would be a reduction in the possibility of infanticide by males, as they would be unable to selectively kill their rivals’ offspring. This hypothesis shows support in the recent studies on wild Hanuman langurs that display concealed ovulation and frequent matings with males outside their fertile ovulatory period. Heistermann et al. hypothesize that concealed ovulation is used by females to confuse paternity and thus reduce infanticide. He explains that since males determine paternity and thus decide on whether to kill the female’s child based on his previous matings with that female, a female’s promiscuous matings in conjunction with concealed ovulation would lead a male to believe that there is still a possibility for that child to be his own.

Sex and Reward Hypothesis

Schroder reviews Symons' and Hill's hypothesis that states that hunting males exchanged meat for sex with females. Females that continuously mimicked estrus may have benefited from more meat than those that did not. If this occurred with enough frequency, then a definite period of estrus would have been lost, and, with it, sexual signaling specific to ovulation would have disappeared.

Social-Bonding Hypothesis

Schroder presents the idea that there was a “gradual diminution of mid-cycle estrous and concomitant continuous sexual receptivity in human women” because it facilitated orderly social relationships throughout the menstrual cycle by eliminating the periodic intensification of male-male aggressiveness in competition for mates. It has been said that the extended estrous period of the bonobo (reproductive-age females are in heat for 75% of their menstrual cycle) has a similar effect to the lack of a "heat" in human females. While concealed human ovulation may have evolved in this fashion of extending estrous until it was no longer a distinct period, as paralleled in the bonobo, this hypothesis for why concealed ovulation evolved has frequently been rejected. Schroder outlines the two objections to this hypothesis: (1) Natural selection would need to work at a level above the individual, which is difficult to prove. (2) Selection, because it acts on the individuals with the most reproductive success, would thus favor greater reproductive success over social integration at the expense of reproductive success.

Cuckoldry Hypothesis

Benshoof and Thornhill hypothesized that estrous became hidden after monogamous relationships became the norm in Homo erectus. Concealed ovulation allowed the female to mate with genetically superior males and thus gain the benefit of their genes for her offspring while still maintaining the pair bond with her lesser male partner. The bonded male would have little reason to doubt her fidelity because of the concealed ovulation and would have high, albeit unfounded, paternity confidence in his offspring. His confidence would encourage him to invest in the child even though it was not his own. Again, the idea of paternal investment being vital to the offspring’s survival, and thus vital to the male and female partner’s fitness is a central fixture of a hypothesis regarding concealed ovulation.

Concealed Ovulation as a Side Effect of Bipedalism

Pawlowski presents the importance of bipedalism to the mechanics and necessity of ovulation signaling. The more open savannah environment inhabited by early humans (as made available by bipedalism) brought greater danger from predators. This would have caused humans to live in more dense groups, and, in such a scenario, the long-distance sexual signaling provided by female genital swellings would have lost its function. Concealed ovulation is thus argued to be a loss of function evolutionary change rather than an adaptation. Thermoregulatory systems were also modified in humans with the move to the savannah in order to conserve water. It is thought that female genital swellings would have incurred added cost because of ineffective evaporation of water from the area. Pawlowski continues by saying that the change to bipedalism in early hominins changed both the position of female genitals and the line of vision of males. Since males could no longer constantly see the female genitals, swelling of them during estrous as a mode of signaling would have become useless. Also, anogenital swelling at each ovulatory period may have interfered with the mechanics of bipedal locomotion, and selection may have favored females who were less hindered by this occurrence. This hypothesis ultimately concludes that bipedalism, which was strongly selected for, caused the physiological changes and a loss of function of sexual signaling through female genital swelling, leading to the concealed ovulation we now observe.

Pawlowski’s paper offers views that differ from the other hypotheses regarding concealed ovulation in that it pinpoints physiological changes in early humans as the cause of concealed ovulation rather than social or behavioral ones. One of the strengths of this is derived from the other hypotheses’ weakness – it is difficult to track the evolution of a behavior as it leaves no verifiable evidence in the form of bone or DNA. However, the fact that the Hanuman langurs also display some concealed ovulation and that it is not directly caused by a physiological change to bipedalism may suggest that bipedalism was not, at least the sole, cause of concealed ovulation in humans. As stated earlier, it is possible for many elements of different hypotheses to be true regarding the selective pressures for concealed ovulation in humans.

References

Sandy J. Andelman (1987). "Evolution of Concealed Ovulation in Vervet Monkeys (Cercopithecus aethiops)". The American Naturalist. 129: 785–799. doi:10.1086/284675. {{cite journal}}: Unknown parameter |month= ignored (help)
S.C. Roberts, J. Havlicek, J. Flegr, M. Hruskova, A.C. Little, B.C. Jones, D.I. Perrett and M. Petrie (2004). "Female facial attractiveness increases during the fertile phase of the menstrual cycle". Proc.R.Soc.Lond.B (Suppl.). 271: S270–S272. doi:10.1098/rsbl.2004.0174. PMC 1810066. PMID 15503991. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
Geoffrey Miller, Joshua M. Tybur and Brent D. Jordan (2007). "Ovulatory cycle effects on tip earnings by lap dancers: economic evidence for human estrous?" (PDF). Evolution and Human Behavior. 28 (6): 375–381. doi:10.1016/j.evolhumbehav.2007.06.002. Retrieved 2008-01-21. {{cite journal}}: Unknown parameter |month= ignored (help)
Pipitone, R. (2008-05-18). "Women's voice attractiveness varies across the menstrual cycle". Evolution and Human Behavior. 29 (4): 268–274. doi:10.1016/j.evolhumbehav.2008.02.001. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
Susan B. Bullivant, Sarah A. Sellergren, Kathleen Stern; et al. (2004). "Women's sexual experience during the menstrual cycle: identification of the sexual phase by noninvasive measurement of luteinizing hormone". Journal of Sex Research. 41 (1): 82–93. doi:10.1080/00224490409552216. PMID 15216427. {{cite journal}}: Explicit use of et al. in: |author= (help); Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
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Motluk, Alison (2006-08-05). "The secret life of semen". New Scientist (2563). Retrieved 2008-06-28. {{cite journal}}: External link in |journal= (help)
Chris Knight (1991). Blood relations: menstruation and the origins of culture. New Haven, Conn: Yale University Press. ISBN 0-300-04911-0.
Knight, Chris (1995). "The Human Symbolic Revolution: A Darwinian Account" (PDF). Cambridge Archaeological Journal. 5 (1): 75–114. doi:10.1017/S0959774300001190. Retrieved 2006-12-13. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
Burt, Austin (1992). "'Concealed ovulation' and sexual signals in primates". Folia Primatologica. 58: 1–6. doi:10.1159/000156600. {{cite journal}}: Unknown parameter |month= ignored (help)
Frederick S. Szalay and Robert K.Costello (1991). "Evolution of permanent estrus displays in hominids". Journal of Human Evolution. 20: 439–464. doi:10.1016/0047-2484(91)90019-R. {{cite journal}}: Unknown parameter |month= ignored (help)
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