In
nonhuman primates, similar to other mammals, during the female’s cycle,
sex steroid hormones are regulated by the release of the pituitary
gland peptides follicle-stimulating hormone (FSH) and luteinizing
hormone (LH). FSH stimulates the growth of the sex cells, the ovarian
follicles; LH in high concentrations induces ovulation in Graafian
follicles that have been primed with FSH. Data on rhesus macaques show
that preovulatory LH and FSH peaks affect estradiol increases and thus
represent important prerequisites for a successful ovulation (Dixson
1998). More than 40 years ago, Dixson et al. (
1973)
reported not only a periovulatory increase of estradiol in primates,
but also a similar peak of the androgen testosterone. Later, Nadler et
al. (
1985)
demonstrated an association between estradiol and testosterone
concentrations during the mid-cycle phase and maximum perineal swelling
size in the common chimpanzee. Moreover, the mid-cycle estradiol and
testosterone peaks in chimpanzees are comparable to those in women
(Morris et al.
1987).
The Three-Fold Impact of SSC in Nonhuman Primates: Attractiveness, Fertility, and Sociality
Females
of many nonhuman primate species exhibit sexually attractive signals
during their cycle. The most prominent signals are coloration and/or
perineal swelling. The coloration and degree of anogenital swelling size
may affect the vulva area, the clitoris, to some extent the perineal
region, and the area around the ischial callosities (Dixson
1983).
Both coloration and perineal swelling can vary dramatically among
females in a group. Their expression rates are controlled by the sex
steroids estradiol and progesterone. Estradiol enlarges swellings by
transferring water into the intercellular tissue, and an increased blood
flow causes more intensive coloration (Bradley and Mundy
2008). After ovulation, the luteal steroid progesterone reduces the swellings (Wildt et al.
1977).
Both the intensity of coloration and the size of the swelling are most
pronounced during the periovulatory period (Wallner et al.
2011; Möhle et al.
2005).
These
periods are correlated with the highest copulation frequencies, and the
probability of fertilization is highest as well. Nonetheless, studies
on Barbary macaques indicate that sexual interactions are not limited to
the periovulatory period and are therefore displayed independently of
the probability of fertilization, e.g., pregnant females with perineal
swellings can copulate as much as non-pregnant ones (Küster and Paul
1984).
However, fluctuations in swelling size and/or coloration are often
correlated with low sex hormone secretion rates and with sexual
behavior. Lactating females too can show sexual solicitation behavior
and copulations (Brauch et al.
2007).
A comparison between non-lactating and lactating females in Japanese
macaques revealed more intensive red coloration and copulations (with
and without ejaculations) for non-lactating females during sexually
active periods (Wallner et al.
2011).
However, copulations (with and without male ejaculation) were not
uncommon among lactating females, although they showed slight changes in
coloration intensity and their sex steroid production was significantly
lower compared to non-lactating females. Less well-understood is the
functional significance of changes in coloration intensity and size of
the perineal swellings in Tibetan macaques, as females in this species
do not exhibit any typical behavior associated with estrus and they
copulate frequently outside the mating season (when SSC are not
obviously expressed) (Li et al.
2005,
2007).
Non-reproductive copulations were not observed in pregnant or lactating
individuals and typically involved adolescent males. Such copulations
often occurred after social conflicts, whereby females approached males
and solicited copulation, suggesting a social function of sexual
behavior (Li et al.
2007).
Ovariectomy does not suppress female sexual behavior in Old and New World monkeys. In stumptail (Baum et al.
1978) and rhesus macaques (Chambers and Phoenix
1987) ovariectomized females show some sexual receptivity, and in the common marmoset (Kendrick and Dixson
1984)
males still exhibit high copulation frequencies with ovariectomized
females. Baboon females that had been ovariectomized hardly drew the
attention of singly housed males when placed in visual, olfactory, and
auditory contact with them (Girolami and Bielert
1987).
Nonetheless, if the same females were provided with large artificial
swellings, then the males became sexually aroused and masturbated.
Masturbation is not unique to humans (Dixson
1998), but self-stimulation of genitalia is nearly exclusively reported in Old World monkeys and apes (Dubuc et al.
2013).
This type of behavior is shown under captive, semi-free, and wild
conditions. Barbary macaque females implanted with contraceptives
exhibit perineal swellings during non-sexual periods. Males seemed to be
more attracted to females with enlarged swellings (Wallner et al.
1999).
They inspected — sniffed and touched — the anogenital region of these
females and masturbated frequently in their presence. Almost no mounting
behavior was performed, suggesting that visible sexual traits stimulate
self-directed sexual behavior in males (Wallner, pers. obs.).
A
study on same-sex mounting behavior in Japanese macaque females showed
that females were able to self-stimulate their vulvar, perineal and anal
(VPA) regions. Females also mounted other females and while doing so,
they rubbed their VPA on their partners or stroked their VPA with their
own tail (Vasey and Duckworth
2006).
Because the VPA region mediates sexual arousal in both humans and in
nonhuman primates, the authors of this study interpreted the behavior of
macaque females as providing an immediate sexual reward. Such sexual
sensation from genitalia activates the mesolimbic brain areas
(Georgiadis and Kringelbach
2012),
resulting in the perception of pleasure. Early research suggested that
nonhuman primates mate exclusively in a dorso-ventral position, whereas
humans prefer face-to-face sexual intercourse to facilitate female
orgasm. Early studies also suggested that that nonhuman primate females
are not able to experience orgasm. Both suggestions proved wrong: lesser
and great apes engage in face-to-face copulation, and female orgasm has
been recently reported in a number of monkey species (Dixson
2009).
Bonobos
display unique patterns of socio-sexual behavior for nonhuman primates.
In bonobos, sexual interactions occur daily, and independent of female
cycle stages and therefore of reproduction. Sexual interactions involve a
variety of sexual behaviors and include individuals of all age and sex
combinations (Manson et al.
1997). Chimpanzees also exhibit perineal swellings beyond ovulation periods. Wallen and Zehr (
2004) noted
,
“The system of hormonally modulated sexual motivation combined with a
physical capacity to mate at any time has evolved in primates to balance
the social and reproductive uses of sex.” This clearly applies to
female sexuality in great apes such as bonobos and chimpanzees. In
orangutans, females do not express SSC, suggesting that ovulation is
concealed (Pawlowski
1999). Knott et al. (
2010)
investigated sexual interactions in Bornean orangutans. Near ovulation,
females copulated with dominant, flanged males with large cheek pads,
but during cycle stages with low probability of fertilization, females
preferred less dominant, unflanged males. The authors suggested that in a
species with concealed ovulation where males use frequent sexual
coercion, such female sexual strategies may minimize male aggression.
Differentiated female preferences for mating with adult and adolescent
males at different cycle stages was also reported in Phayre’s leaf
monkeys. During periovulatory periods (POP), females were more
proceptive and receptive to adult males, but they preferred adolescent
males during non-periovulatory periods (NPOP). Interestingly, adult
males seemed to recognize female fertility better than adolescent
individuals did (Lu et al.
2012).
Another study investigated female chimpanzee mating preferences during
POP and NPOP. Female proceptivity correlated with male mating success
and female resistance behavior reduced male mating success, during POP.
Proceptivity was also positively related with male mating success during
NPOP. These data indicate the influence of female choice on male mating
success during different cycle stages in chimpanzees (Stumpf and Boesch
2006).
In white-handed gibbons, cycling females showed increased group-leading
activities compared to pregnant or lactating females. The behavior
probably served a non-ecological function, and helped females search for
potential mating partners (Barelli et al.
2007).
Female
SSC-related signals are attractive to males and may stimulate male
sexual arousal. Females, in turn, may benefit from received increased
social and sexual attention from males. For example, Barbary macaque
females implanted with contraceptives can develop enlarged swellings
during non-reproductive periods and, if so, they have more affiliative
interactions and fewer agonistic interactions with males, and they
receive more agonistic aid and more grooming from males (Wallner et al.
1999,
2006).
Similarly, female chimpanzees with swellings enjoy significantly more
social benefits than those without swellings. In addition to their
increased affiliative interactions with males, they gain greater access
to food resources. Pregnant chimpanzee females with large perineal
swellings may find it easier to transfer from one group to another
without being attacked by males (Wallis
1982,
1992). Furthermore, baboon males strategically approach swollen females when entering a new group (Goodall
1986), and affiliate temporarily with them.
Why
males find SSC signals attractive is more difficult to interpret. In
other words, the information content, if any, of these signals remains
unclear. Pagel (
1994)
argued that large perineal swellings are reliable indicators of female
reproductive quality and health. Such signals must be the evolutionary
result of intra-sexual female competition for males. This reliable
indicator hypothesis was supported by data from wild olive baboons,
showing that females that exhibited larger swellings during their
sexually active periods had more affiliative interactions with males and
produced more offspring than females with smaller swellings (Domb and
Pagel
2001).
Critics of this study, however, were able to show major flaws in the
statistical data analyses. Subsequent studies failed to replicate these
results and to show better reproductive performance for females with
larger swellings (Setchell et al.
2006a; see Fitzpatrick et al.
2015).
Nevertheless, there are indications that conceptive swellings are
larger than non-conceptive ones and that males do prefer to mate with
females during those cycles with higher chance of fertilization
(Fitzpatrick et al.
2015).
With
regard to coloration, non-lactating Japanese macaque females had more
intense red coloration, especially at the nipple and hindquarter
regions, and all of them conceived during the sexually active period
compared to those who were lactating (Wallner et al.
2011).
In mandrills, multiparous females had brighter faces, possibly
signaling their history of successful reproduction and current
fertility, than nulliparous females (Setchell et al.
2006b).
Rhesus macaque males preferred females with more reddened hindquarters,
whereas females paid more attention to faces of males and females with
intense red coloration; the latter may be associated with female-female
competition as well (Gerald et al.
2007; Dubuc et al.
2016).
Similarly, Japanese macaque males were more interested in faces with
more intense red coloration, and especially in faces with increased
color contrast (Pflüger et al.
2014).
Female
SSC signals in relation to ovulation are generally prominent in primate
species that live in multi-male, multi-female groups with promiscuous
mating systems. In contrast, in species that live in one-male units,
with polygynous or monogamous mating systems, SSC signals such as sexual
swellings are rare and seem to be less related to advertising female
fertility. The ultimate reason for such differences seems to be
intrasexual competition for mating partners during periovulatory periods
in promiscuous species compared to one-male units [...exception is the white-handed gibbon...].
Women: Behavioral and Morphological Variation
Women’s sexual behavior may fluctuate significantly during their cycle. Burleson et al. (
2002)
investigated allosexual and autosexual behavior in heterosexual and
lesbian women with or without a partner. Allosexual behavior increased
during the follicular and ovulatory phases in women living with a
partner compared to those without a partner. In contrast, the
frequencies of autosexual behavior were elevated during the follicular
and ovulatory cycle phases in both heterosexual and lesbian women living
without a partner vs those with a partner. A longitudinal study of
female sexual behavior during five cycle phases - namely menstrual,
postmenstrual, ovulatory, luteal and premenstrual - showed peak sexual
activities during ovulation (Harvey
1987).
That study used temperature charts to identify different cycle stages. A
more recent investigation assessed sexual activities in relation to the
preovulatory LH increase. Women initiated more sexual activities during
the preovulatory LH surge and showed increased sexual desire and
fantasies 3 days earlier (Bullivant et al.
2004). Pillsworth et al. (
2004)
showed that sexual desire in paired women was mainly expressed during
the periovulatory phase, and that among these women increased conception
probability was correlated with sexual desire. Interestingly, the
duration of partnership was positively related to sexual desire in
extra-pair-relationships during periods of increased fertility. Another
study on sexual fantasies in relation to menstrual cycle phases in
single-living women showed increased sexual fantasies during
preovulatory elevated LH secretion; these fantasies decreased after
ovulation (Dawson et al.
2012).
During follicular and periovulatory periods the number of sexual
fantasies increased while emotional content increased in conjunction
with ovulation (Dawson et al.
2012).
It
has been argued that during fertile cycle phases, paired women may
engage in short-term extra-pair relationships to mate with partners of
high genetic quality (such as high testosterone levels, masculinity,
dominance, symmetry) (e.g., Gangestad and Thornhill
2008). Two recent meta-analyses of these studies, however, provided mixed support this conclusion (Gildersleeve et al.
2014; Wood et al.
2014) and subsequent, rigorous investigations have failed to replicate some of the initial findings (Jones et al.
2018a,
b; Jünger et al.
2018).
Evidence concerning the influence of hormones on sexual desire during
different cycle stages seems to be also conflicting. Roney and Simmons (
2016)
found a significant negative correlation between progesterone increases
and women’s desire for their partner and other men. In contrast,
mid-cycle stages were related to high extra-pair and in-pair desire,
although the correlation between desire and estradiol was only
marginally significant. Contrary to these results, another study showed
that higher estradiol levels are associated with an increased extra-pair
sexual interest, whereas higher progesterone concentrations predict
greater in-pair interest (Grebe et al.
2016).
Finally, recent studies have provided some further conflicting evidence
as to whether changes in estradiol and progesterone concentrations
across the cycle are associated with changes in female general sexual
desire vs female desire for particular types of sexual relationships
(Jones et al.
2018a; Shirazi et al.
2019).
Many
studies of women’s mate preferences in relation to the menstrual cycle
compare fertile vs luteal phases. During fertile periods, women do
generally prefer masculine men who are assertive and competitive, have
lower voices, or scents associated with body symmetry (Gangestad et al.
2004; Garver-Apgar et al.
2008).
For example, in one study, women’s preference for male scents related
to symmetric body features was positively related to women’s estrogen
and testosterone levels, but negatively to their progesterone
(Garver-Apgar et al.
2008).
Furthermore, women with lower urinary estrone-3-glucuronide
concentrations showed stronger cyclic shifts (non-fertile/fertile) in
their preferences for masculine voices (Feinberg et al.
2006; but see Jünger et al.
2018
for negative results). Finally, cycle stage apparently plays an
important role in being motivated to detect erotic stimuli in art.
During the first half of the menstrual cycle, women emphasized more
erotic stimuli in paintings compared to the second half of the cycle
(Rudski et al.
2011).
Aside from behavioral changes, different energetic needs are also evident during the menstrual cycle. Lissner et al. (
1988)
described two peaks of energy intake during the cycle: the first at the
middle of the follicular phase, and the second at the middle of the
luteal phase. Especially during the luteal phase, women crave more
carbohydrate- and fat-containing food (Davidsen et al.
2007).
From a physiological point of view, such food consumption behavior is
relevant because energy is needed to produce the endocrine surges
necessary for ovulation and for the successful implantation of
fertilized eggs into the uterus tissue. Another study showed that
consuming sweet food and its preference rating increase during the
pre-ovulatory phase (Bowen and Grunberg
1990).
Both, nonhuman primates and humans, however, show increased luteal
energy intake compared to follicular phases (Dye and Blundell
1997). Czaja and Goy (
1975)
carried out classical studies on food intake under estrogen and
progesterone treatment in rhesus macaques and guinea pigs. In both
species, the food intake decreased around the time of ovulation and
increased during other cyclic periods. Estrogen administration to
ovariectomized females showed a clear downregulation of feeding
behavior. Ovariectomized females, however, did not change their feeding
behavior after progesterone administration compared with control
individuals in both species. Most recently, Roney and Simmons (
2017)
tested hormonal predictors of daily self-reported food intake in
naturally cycling women. They reported that estradiol negatively and
progesterone positively predicted food intake, and that a decrease in
eating during the fertile phase of the cycle was mediated by the two
hormones. These associations between hormones and food intake were
mirror images of those found for sexual desire, and were very similar to
those reported in nonhuman primates.
In
addition to sexual desire/preferences and food intake, a great deal of
research has documented also changes in mood and cognitive function in
relation to the menstrual cycle. Some of this research has involved
estrogen replacement therapy (reviewed by Shively and Bethea
2004; see also Voytko
2002,
for data in female macaques). In women, the premenstrual syndrome and
its association with depression are relatively well investigated (e.g.,
Forrester-Knauss et al.
2011). Interestingly, Shively et al. (
2002) were able to relate lower ovarian function and impaired HPA activity with signs of depression in subordinate macaque females.
Risky Behavior During Menstrual Cycle
Sexual interactions are per se related to physical risks for both sexes (Wallen and Zehr
2004).
For example, T lymphatic viruses are sexually transmitted in humans and
in several species of nonhuman primates (see Junglen et al.
2010).
Simian and human immunodeficiency viruses (SIV, HIV) are among the most
infamous sexually transmitted diseases. The Center for Disease Control
and Prevention (
https://www.cdc.gov/)
has indicated that in the U.S. individuals between 15 and 24 years of
age represent 27% of the sexually active population, yet they account
for 50% of sexually transmitted infections. In their fact sheet of
infections, gonorrhea ranks number one (70%) followed by chlamydia
(63%), HPV (49%), genital herpes (45%), HIV (26%), and syphilis (20%).
These data, however, do not reveal whether infections are related to
specific menstrual cycle stages. Regarding the type of infection, women
in the 15–24 years range seem to be most vulnerable to chlamydia
infections. Interestingly, some of these pathogens - such as chlamydia (
Chlamydia trachomatis) or syphilis (
Treponema pallidum) – have also been detected in captive apes (Rushmore et al.
2015), although little research on sexually transmitted diseases has been conducted in wild nonhuman primates.
Molecular
immune defense genes seem to evolve faster in promiscuous primate
species, and especially in species that live in larger groups (Wlasiuk
and Nachman
2010). Nunn et al. (
2000)
found that white blood cell counts were significantly higher in primate
species in which females have more mating partners, and therefore the
risk of sexually transmitted diseases is higher. A recent study analyzed
the evolution of the seminal protein gene semenogelin 2 (SEMG2) in
primates, which is responsible for the semen coagulation rate (Dorus et
al.
2004).
The results showed that promiscuous species exhibit higher rates of
SEMG2 polymorphism, which results in faster coagulation rates. The
species with the highest evolution rate is the common chimpanzee.
Interestingly, the relationship between the rate of evolution of SEMG2
and residual testis size is higher in humans than in polygynous
(orangutan, gorilla) or monogamous (gibbon) species (Dorus et al.
2004).
A similar correlation is evident between midpiece sperm volume (the
location of mitochondria) and residual testis size in humans (Anderson
and Dixson
2002).
Both results indicate a selection process favoring moderate promiscuity
in humans. Based on these findings and the previously mentioned female
desire for extra-pair sex during fertile cycle stages, it may be argued
that women’s fertility periods are associated with risky behavior.
In
female baboons, an increased risk of injury (presumably related to
reproductive competition) has been documented during days with a high
conception probability (Archie et al.
2014).
Promiscuous female baboons signal their periovulatory period with
exaggerated swellings, which may attract the males’ sexual attention but
also aggression from males and females. Women seem to have developed
strategies to reduce their exposure to risk during fertile cycle
periods. During ovulation, women engage in less risky behaviors to avoid
sexual assaults (Bröder and Hohmann
2003)
and show an increase in handgrip strength in response to a sexual
assault vignette, suggesting the existence of behavioral adaptations to
reduce the probability of conception as a result of rape (Petralia and
Gallup
2002).
However, strong individual differences probably exist among women in
their tendency to engage in sex-related risky behavior in relation to
their age, personality, chronotype (i.e., morningness-eveningness), and
hormonal profiles (e.g. Maestripieri
2014).
It is possible that variation in female risky behavior during the cycle
may be influenced by cortisol and its interaction with sex hormones. A
study on a rural Mayan population showed increased urinary cortisol
during the follicular phase and between day 4 and 10 after ovulation.
Interestingly, higher cortisol during the follicular phase was
associated with progestin concentrations, suggesting an impairment of
implantation processes (Nepomnaschy et al.
2004).
Women’s Advertising During Different Cycle Phases
Do
human females differ from other primate females in advertising their
sexual attractiveness in relation to different cycle stages? In contrast
to some primate SSC signals such as exaggerated sexual swellings, which
fluctuate across the cycle in relation to changes in estrogen and
progesterone concentrations (Wallner et al.
2006,
2011),
women have permanent developed SSC such as the waist-to-hip ratio,
buttocks, and breasts. Nonetheless, cyclic changes in body morphology
are evident also in women (reviewed in Farage et al.
2009).
Most of these changes are related to physiological parameters such as
lipid content of skin, collagen production, pigmentation, hydration,
thermoregulation, functional aspects of the immune system or changes of
water compartments and subcutaneous fat tissue. Whether these cyclic
modifications are detectable by men remains unclear (Puts et al.
2013; for evidence, instead, that cyclic modifications in faces are detectable by women, see Necka et al.
2016,
2018; Hurst et al.
2017; Krems et al.
2016).
Some of the most obvious changes occur in the subcutaneous fat regions of the thighs and abdomen (Perin et al.
1999).
In these areas, fat increases up to 4% during menstruation, and the fat
content is lowest during the first half (follicular stage) of the
cycle. Fowler et al. (
1990)
used magnetic resonance imaging to detect changes in the female breast
volume during the cycle. During the period between day 16 and 28, which
more or less corresponds to the luteal phase, the water content
increased by 24%, and parenchymal volume by 38%. In comparison, during
menstruation, water content decreased by 17%, and parenchymal volume by
30%. This represents a major volume change for the breast tissue, which
is analogous to changes in anogenital swellings in nonhuman primates.
However, the volume increase in swellings is mediated by estrogens and
is based on a shift of intracellular water into the interstitial tissue,
whereas the volume increase in the breast tissue seems to be mediated
by luteal progesterone. Whether these subcutaneous fat changes during
the cycle are temporal SSC, which signal attractiveness in women remains
unclear.
There are, however, hints that
women try to enhance their sexual attractiveness during particular
phases of the cycle. A study on more than 300 women revealed some
associations between clothing preferences, sexual motivation, and
hormone concentrations (Grammer et al.
2004).
Higher sexual motivation was associated with the tendency to wear sheer
clothing (which allows the woman’s body or undergarments to be seen
through its fabric), whereas salivary estradiol concentrations were
correlated with the amount of skin exposure and with clothing tightness.
Moreover, women significantly change their consumer behavior across the
cycle and spend more time and money on cosmetics, fashion, and jewelry
during the periovulatory phase (Durante and Griskevicius
2016; Durante et al.
2010).
There is also some evidence that these changes in behavior are
influenced by hormones and that they reflect female-female competition
for mating partners (Durante and Griskevicius
2016; Durante et al.
2010).
These
findings indicate that women are aware of their cycle stage and use
their clothes or make-up to attract men’s attention on particular body
regions such as their lips, breasts, or hips (see Haselton and
Gildersleeve
2011).
Gait also changes during the cycle, such that particular postures are
used that help advertise SSC such as the waist and hips. Guéguen
2012showed
that during the periovulatory phase women walk more slowly and that men
find this sexier, suggesting that gait is a critical behavior used by
women to display and enhance their physical attractiveness. Wearing
shoes with high heels may influence the walking performance of women
during periovulatory cycle stages. Wearing high heels enables women to
change significantly the lumbar curvature and the inclination of the
pelvis (Smith
1999).
Visually, this yields a posture signaling a hollow-back and exposing
the waist and hips more prominently. Evidently, men recognize it as a
supernormal stimulus and associate it with female attractiveness. High
heels also influence the gait of women by reducing stride length and
increasing the rotation of the hip.
In
conclusion, advertising physical attractiveness is an important adaptive
trait in the context of sexual interactions in many nonhuman primates
and in humans. [
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