Concealed ovulation or hidden estrus
in a species is the lack of any perceptible change in an adult female
(for instance, a change in appearance or scent) when she is fertile and
near ovulation. Some examples of perceptible changes are swelling and redness of the genitalia in baboons and bonobos, and pheromone release in the feline family. In contrast, the females of humans and a few other species that undergo hidden estrus have few external signs of fecundity,
making it difficult for a mate to consciously deduce, by means of
external signs only, whether or not a female is near ovulation.
Human females
In
humans, an adult woman's fertility peaks for a few days during each
roughly monthly cycle. The frequency and length of fertility (the time
when a woman can become pregnant) is highly variable between women, and
can slightly change for each woman over the course of her lifespan.
Humans are considered to have concealed ovulation because there is no
outward physiological sign, either to a woman herself or to others, that
ovulation, or biological fertility, is occurring. Knowledge of the
fertility cycle, learned through experience or from educational sources,
can allow a woman to estimate her own level of fertility at a given
time (fertility awareness).
Whether other humans, potential reproductive partners in particular,
can detect fertility in women through behavioral or invisible biological
cues is highly debated. Scientists and laypersons are interested in
this question because it has implications for human social behavior, and
could theoretically offer biological explanations for some human sexual
behavior. However, the science here is weak, due to a relatively small
number of studies.
Several small studies have found that fertile women appear more
attractive to men than women during infertile portions of her menstrual
cycle, or women using hormonal contraception. It has also been suggested that a woman's voice may become more attractive to men during this time. Two small studies of monogamous
human couples found that women initiated sex significantly more
frequently when fertile, but male-initiated sex occurred at a constant
rate, without regard to the woman's phase of menstrual cycle. It may be that a woman's awareness of men's courtship signals
increases during her highly fertile phase due to an enhanced olfactory
awareness of chemicals specifically found in men's body odor.
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 menstruation itself).
This is contrary to other studies, which have found female sexual
desire and extra-pair copulations (EPCs) to increase during the
midfollicular to ovulatory phases (that is, the highly fertile phase).
These findings of differences in woman-initiated versus man-initiated
sex are likely caused by the woman's subconscious awareness of her
ovulation cycle (because of hormonal changes causing her to feel
increased sexual desire), contrasting with the man's inability to detect
ovulation because of its being "hidden".
In 2008, researchers announced the discovery in human semen of hormones usually found in ovulating women. 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 this phenomenon may be
a human 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
Evolutionary psychologists have advanced a number of different possible explanations for concealed ovulation.
Some posit that the lack of signaling in some species is a trait
retained from evolutionary ancestors, 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 (regarding humans specifically) is that while
highly specific signaling of ovulation is absent, human female anatomy
evolved to mimic permanent signaling of fertility.
Paternal investment hypothesis
The paternal investment hypothesis is strongly supported by many evolutionary biologists. Several hypotheses regarding human evolution integrate the idea that women 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 women concealed ovulation to obtain men's aid in rearing offspring. Schoroder[14]
summarizes this hypothesis outlined in Alexander and Noonan's 1979
paper: if women no longer signaled the time of ovulation, men would be
unable to detect the exact period in which they were fecund. This led
to a change in men's mating strategy: rather than mating with multiple
women in the hope that some of them, at least, were fecund during that
period, men instead chose to mate with a particular woman repeatedly
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 evolutionarily successful. A similar hypothesis was proposed by Lovejoy in 1981 that argued that concealed ovulation, reduced canines and bipedalism evolved from a reproductive strategy where males provisioned food resources to his paired female and dependent offspring.
Continuous female sexual receptivity
suggests 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 woman is pregnant or
in the infertile period of her menstrual cycle do not achieve
conception, but do strengthen the bond between these partners.
Therefore, the increased frequency of copulations due to 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, lactation and caring for
post-lactation offspring require vast amounts of energy and time on the
part of the woman. She must at first consume more food, then provide
food to her offspring, while her ability to forage is reduced
throughout. Supplemental male investment in the mother and her
offspring is advantageous to all parties. While the man supplements the
woman's limited gathered food, the woman is enabled to devote the
necessary time and energy to the care of their 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 man and
woman would increase their offspring's chances for survival, thereby
increasing their reproductive fitness. In this way natural selection
would favor the establishment of pair bonds in humans. To the extent
that concealed ovulation strengthened pair bonding, selective pressure
would favor concealed ovulation as well.
Another, more recent, hypothesis is that concealed ovulation is
an adaptation in response to a promiscuous mating system, similar to
that of our closest evolutionary relatives, bonobos and chimpanzees.
The theory is that concealed ovulation evolved in women to lessen
paternity certainty, which would both lessen the chances of infanticide
(as a father is less likely to kill offspring that might be his), and
potentially increase the number of men motivated to assist her in caring
for her offspring (partible paternity). This is supported by the fact that all other mammals with concealed ovulation, such as dolphins and gray langurs,
are promiscuous, and that the only other ape species that have
multi-male communities, as humans do, are promiscuous. It is argued that
evidence such as the Coolidge effect,
showing that a man does not seem to be naturally geared towards sexual
mate-guarding behavior (that is, preventing other males from having
access to his sexual partner), supports the conclusion that sexual
monogamy (though perhaps not social monogamy and/or pair bonding) was rare in early modern humans.
Reduced infanticide hypothesis
This hypothesis suggests the adaptive advantage for women who had hidden estrus would be a reduction in the possibility of infanticide by men, as they would be unable to reliably identify, and kill, their rivals' offspring. This hypothesis is supported by recent studies of wild Hanuman langurs, documenting concealed ovulation, and frequent matings with males outside their fertile ovulatory period. Heistermann et al. hypothesize that concealed ovulation is used by women to confuse paternity and thus reduce infanticide in primates.
He explains that as ovulation is always concealed in women, men can
only determine paternity (and thus decide on whether to kill the woman's
child) probabilistically, based on his previous mating frequency with
her, and so he would be unable to escape the possibility that the child
might be his own, even if he were aware of promiscuous matings on the
woman's part.
Sex and reward hypothesis
Schoroder
reviews a hypothesis by Symons and Hill, that after hunting, men
exchanged meat for sex with women. Women who 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
Schoroder
presents the idea of a "gradual diminution of mid-cycle estrus 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.
The extended estrous period of the bonobo (reproductive-age females are
in heat for 75% of their menstrual cycle) has been said to have a
similar effect to the lack of a "heat" in women. While concealed human
ovulation may have evolved in this fashion, extending estrus until it
was no longer a distinct period, as paralleled in the bonobo, this
theory of 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; and (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.
However, since 1993 when that was written, group selection models have seen a resurgence.
Cuckoldry hypothesis
Schroder
in his review writes that Benshoof and Thornhill hypothesized that
estrus became hidden after monogamous relationships became the norm in Homo erectus.
Concealed ovulation allowed the woman to mate secretly at times with a
genetically superior man, and thus gain the benefit of his genes for
her offspring, while still retaining the benefits of the pair bond with
her usual sexual partner. Her usual sexual partner would have little
reason to doubt her fidelity, because of the concealed ovulation, and
would have high, albeit unfounded, paternity confidence in her
offspring. His confidence would encourage him to invest his time and
energy in assisting her to care for the child, even though it was not
his own. Again, the idea of a man's investment being vital to the
child's survival is a central fixture of a hypothesis regarding
concealed ovulation, even as the evolutionary benefits accrue to the
child, the woman, and her clandestine partner, and not to her regular
sexual partner.
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 brought greater danger
from predators. This would have caused humans to live in denser 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
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 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 estrus 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'
weaknesses – 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 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.
