Abstract
Objective and Methods: This review focuses on comparative data in nonhuman primates and humans in relation to signaling secondary sex characteristics (SSC), sexual behavior, and neurophysiology of sexuality during the female cycle.
Results: In monkeys and apes no clear distinction can be drawn between sex as a reproductive, social, or a pleasurable activity. Although female sexual behavior is not limited to a specific phase of the menstrual cycle, changes in body morphology and in behavior and psychology (for example, in feeding, risk taking, and mood) can occur across the cycle. In human and nonhuman primates, homologous biological mechanisms including specific areas of the brain, sex steroids, and receptors are involved in regulating female sexuality. Important aspects of this regulation include the interaction between the subcortical reward system and the social brain network and its projection to the prefrontal cortex. In humans, females advertise SSC permanently after the onset of puberty, but without significant changes across the cycle, whereas in other primate species, female sexual signaling can vary significantly across cycle stages and in fertile and non-fertile phases of the life cycle.
Conclusion: A great deal is now known about the regulation of female sexuality in primates and the use of sexual signals in terms of their variable expression and their information content for males. Human research has also elucidated the cultural mechanisms through which women communicate about their sexuality, including clothes and make-up. A full understanding of female sexuality in humans, therefore, requires knowledge of culture-biology interactions.
Keywords: Comparative primatology Sexual attractiveness Neurophysiological organization Behavior
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Introduction
Female
ovarian cycles have been thoroughly studied in many species of mammals.
A great deal of research on endocrine mechanisms in relation to
behavioral expression rates throughout different cycle stages has
elucidated both the proximate regulation and the functional significance
of female sexual and reproductive strategies in mammals. Female
sexuality involves complex interactions between neuroendocrine
mechanisms in relation to neurotransmitter activities to modulate
behavior. Such neurophysiological processes are only partially
understood in primates.
In most mammals,
sexual activities are limited to the periovulatory period of the female
cycle. This period is characterized by elevated estrogen concentrations
leading to ovulation, followed by an increase of progesterone secretion
that facilitates the implantation of the egg into the uterus. In
general, sexual activity is correlated with estrogen increase and is
reduced at elevated progesterone levels. The period of the cycle in
which females are sexually receptive and sexually active is termed
estrus.
The best-investigated female sexual
behavior in terms of physiology and neurobiology is the lordosis reflex
in rodents. This is a posture in which females allow male intromission.
Shortly before ovulation, males approach their mating partners and
mount them. This sensory interaction enables the lordosis reflex, which
is controlled by the sex steroids estradiol and progesterone. The
behavioral aspect of this reflex is regulated by subcortical
hypothalamic brain structures such as the ventromedial nucleus and the
periacqueductal gray, where ovarian hormones find acting sites to
facilitate the reflex (Flanagan-Cato 2011; Uphouse 2014).
The regulation of lordosis behavior involves complex neurobiological
circuits and their underlying neurochemistry. As illustrated by Beach (1976),
females advertise their sexual readiness to males with their
attractiveness, followed by proceptivity (behavioral signals to males
such as solicitation to copulate), and then by receptivity to copulatory
behavior with subsequent ejaculation.
These
three aspects of female sexuality are related to hormonal changes
during the female cycle and ultimately serve the process of
reproduction. The Beach paradigm was thought to encompass more or less
all non-primate mammalian species. In primates, instead, it has long
been known that females do not limit their sexual behavior to specific
cycle stages and to the corresponding hormone fluctuations (Dixson 2009). In humans in particular, copulations can occur during all cycle stages (Dixson 2009).
This has led some to believe that human sexuality is completely
emancipated from its biological regulation and entirely dependent on
volitional and cultural factors. It is, however, very unlikely that
humans continued to evolved by natural selection up to the Pleistocene,
but then suddenly stopped after settling and farming (approx.
10,000 years ago). Rather, it is more likely that cultural and genetic
processes mutually interacted throughout all human evolution (Richerson
et al. 2010). Natural selection is still acting on certain traits in contemporary humans (Byars et al. 2009)
and producing adaptations through culture-gene co-evolution. This
process may operate much more quickly than previously thought (Field et
al. 2016).
Although there are some important differences between human female
sexuality and female sexuality in nonhuman animals, the prevalent view
emphasizes continuity rather discontinuity between humans and other
animals, especially other primates. Therefore, in this article, we
highlight the many similarities between humans and nonhuman primates in
hormone secretions, neurophysiological subcortical organization, and
female sexual behavior during the reproductive cycle, with particular
emphasis on the signaling of Secondary Sexual Characteristics (SSC).
Hormones, Behavior and SSC
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. [
Neurophysiology of Sexual Behavior
The eighteenth century Venetian Giacomo Casanova stated, “Only
man is capable of real pleasure, because he is gifted with the power of
thought, and he expects the desire, he studied it, he gives and
remembers her, if he has enjoyed it (https://www.aphorismen.de/zitat/67814).
Casanova suggests that three main aspects of human sexuality are
pleasure, desire, and thought, and implies that human beings are perhaps
unique in the animal kingdom in that for humans, sex in mainly in the
brain. In reality, the neurophysiological regulation of sexuality shares
many similarities in humans and other primates. Pleasure and desire are
mainly located in subcortical midbrain structures, which are homologous
among primates. Therefore, it is likely that the way human beings
desire sex and experience sexual pleasure is very similar to the other
primates do it. With regard to thinking about sex, especially conscious
thinking, the situation is more complicated, as humans are unique among
the primates for having a large neocortex that allows for conscious
thinking. The phylogenetic increase in the size of the neocortex from
monkeys to apes to humans seems to be related both to the rate of
neuronal projections from the midbrain to the neocortex as well as to
how the neocortex has evolved (Raghanti et al. 2008).
The
vertebrate brain has several areas that regulate the emotional aspects
of sex as well as the performance of sexual acts. The comprehensive
comparative analysis by O'Connell and Hofmann (2011)
pointed out that brain regions representing the social behavior network
and the mesolimbic reward system are particularly important for the
sensation of pleasure. The size of the hypothalamic nuclei in the social
behavior network is sexually dimorphic. The larger male nucleus of the
preoptic area (POA) and the bed nucleus of stria terminalis (BNST) are
exposed to testosterone during ontogenetically sensitive periods (Hofman
and Swaab 1989).
Such exposure produces concentration-dependent androgen receptor
fields, which are essential for promoting male reproductive behaviors
during adulthood. An important functional role of the POA is to
integrate external and internal information to facilitate mating
behavior and gender identity (Garcia-Falgueras et al. 2011).
Research on female macaques has revealed neuronal activity in the
ventromedial hypothalamus (VMH) and POA areas during sexual activity
(see Dixson 2009). The sex drive in humans and in nonhuman primates is regulated by both androgens and estrogens (Fisher et al. 2006; but see Cappelletti and Wallen 2016).
A dopaminergic influence in the POA on sexual arousal has also been documented (Schober and Pfaff 2007).
The mesolimbic reward system is one of the best investigated brain
areas in medicine and biology. Comparative studies on fishes,
amphibians, reptiles and mammals have revealed analogous functional
neuroanatomic structures (O'Connell and Hofmann 2011). The monoamine neurotransmitter dopamine and its two-class receptor system (Missale et al. 1998; Beaulieu and Gainetdinov 2011)
are key players in these mesolimbic structures. They mediate pleasure
associated with predictive, motivational or attentional sensations in
relation to learning processes (Berridge and Kringelbach 2008).
The dopaminergic system is linked to the prefrontal cortex to mediate
cognitive processes generated subcortically in association with
sex-related emotion and behavior. In the prefrontal cortex, the enzyme
catechol-o-methyltransferase is responsible for deactivating dopamine
(Cumming et al. 1992), while the dopamine transporter protein regulates the duration of dopamine receptor activation (Giros and Caron 1993).
Comparative analyses of cortical dopaminergic innervation in humans and
nonhuman primates reveal no quantitative differences between
chimpanzees, macaques, and humans. However, the sublaminar patterns of
innervation differ in specific areas between humans and the other two
species (Raghanti et al. 2008).
The
main brain structures of the mesolimbic reward system are the striatum
(STR: compulsive behavior), ventral tegmental area (VTA: motivation,
reproduction, parental care), medial amygdala (meAMY: aggression
reproduction, parental care, social recognition), ventral pallidum (VP:
emotional learning, parental behavior), nucleus accumbens (NAcc:
emotional learning, impulsivity, motivation, parental care), and the
hippocampus (HIP: spatial learning) (see O'Connell and Hofmann 2011; Berridge and Kringelbach 2008).
In humans the subcortical and cortical cognitive aspects of sexual
pleasure are related to neural activity in the medial orbitofrontal, mid
insular, and the anterior cingulate areas (de Araujo et al. 2003).
Most of the research on the orbitofrontal cortex has focused on sensory
integration and reward value in relation to food (Kringelbach 2005). According to Rilling (2011)
the reciprocal behavior of food-sharing among non-related
hunter-gatherer populations provides a window into important
neurobiological aspects of human social evolution. fMRI studies
confirmed that the orbitofrontal cortex is also activated during
reciprocal prosocial interactions (Waytz et al. 2012).
We argue that in addition to food-sharing and other prosocial
behaviors, sexual reward also played an important role in the evolution
of the primate orbitofrontal cortex in relation to subcortical brain
areas (see Rudebeck and Murray 2011, and Wikenheiser and Schoenbaum 2016).
Interestingly, both brain areas - the social behavior network and the
reward system - consist of highly interactive nodes and overlapping
structures, which represent an integrated evolutionary ancient social
decision-making network (O'Connell and Hofmann 2011).
Sex Steroid Hormones and their Receptors
Sex
steroid hormones, in particular brain estrogen concentrations,
significantly modulate changes in women’s mood, cognition or sexuality
across the menstrual cycle. The actions of estrogen in the brain depend
on estrogen receptors, which occur in two isoforms: ERα and ERβ. The
latter mediate subcortical cognition processes between hormonal
components and expressed behavior. Patchev et al. (2004)
demonstrated that activating ERα receptors in neonatal female rats
resulted in impaired ovarian function and reduced sexual behavior in
adulthood. This treatment affected the morphology of the subcortical
brain areas such as the periventricular nucleus of the hypothalamus
(AVPV; it produces GnRH in humans and nonhuman primates) and POA,
namely, it made these areas more masculine. In contrast, activation of
ERβ receptors failed to alter later female sexual behavior or
responsiveness to estrogens and did not affect the morphology of the
POA. In situ hybridization in ovariectomized and hysterectomized female
macaques showed the distribution density of ERβ mRNAs for subcortical
hypothalamic, limbic and midbrain areas. Administering estrogens did not
alter overall receptor densities but, progesterone treatment
down-regulated the receptor signal in specific hypothalamic and
hippocampal regions (Gundlah et al. 2000).
Generally, estradiol influences ERα receptors in subcortical areas such
as POA and VMH (both areas belong to social behavior network, which
coordinates sexual activity and is multi-connected with the reward
system) in ewes (Fergani et al. 2014).
Higher estradiol and lower progesterone concentrations are related to
elevated receptor activity and affect sexual behavior under the
influence of an LH surge in both areas (Fergani et al. 2014).
This scenario seems to be typical for mammalian mid-cycle stages.
Similar results were documented for a macaque species, in which estrogen
receptor activity was investigated in several brain areas in mated and
unmated females. Mated females had significantly increased receptor
activities in POA and VMH regions compared to unmated ones (Michael et
al. 2005).
Another primate study focused on the ERα and progesterone receptor
density in hypothalamic regions of ovariectomized aged and young rhesus
macaque females after long-term estradiol treatment. The hormonal
treatment mimicked therapeutic supplements in peri-menopausal women.
Surprisingly, old macaque females maintained estrogen receptor
expression, and long-term estradiol supplementation only marginally
influenced the receptor density (Naugle et al. 2014).
In humans, there is evidence that brain masculinization is AR
(androgen-receptor)-mediated rather than ER-mediated but the issue
remains controversial (Luoto and Rantala 2018; Motta-Mena and Puts 2017; Puts and Motta-Mena 2018).
The
impact of estrogen on the central dopaminergic system and on the brain
reward system is also significant. Menopausal women more often exhibit
symptoms of Parkinson and schizophrenia diseases, which are related to
decreased dopamine production or transmission rates compared to
individuals with cycling estrogen fluctuations (Cyr et al. 2002).
Moreover, decreased dopamine release also seems to be related to the
development of drug addiction. Accordingly, Lynch et al. (2002)
indicated that in adults drug abuse is more likely in males than in
females; in adolescent individuals, however, drug addiction is only
marginally different between the sexes. Studies of self-administration
of alcohol in rats and vervet monkeys showed that females consume higher
amounts of alcohol than males. In rhesus macaques, however, the sex
difference was reversed (Lynch et al. 2002).
Short-term self-administration of heroin did not differ in in male and
females rats. In contrast, extended access to this drug was associated
with higher self-administration in females (Lynch et al. 2002). Cycling women show a dependence of euphoria on d-amphetamine
with regard to behaviors such as liking, wanting, or energy, and
intellectual improvements during later follicle periods (Justice and de
Wit 1999).
Moreover, estradiol seems to improve subjective feelings of pleasure
and feeling “high” in association with amphetamine (Sofuoglu et al. 1999). Nicotine withdrawal, instead, correlated with premenstrual symptoms during the late luteal phase of the cycle (Allen et al. 2000).
These and other studies have shown that estradiol decreases the
dopamine reuptake and therefore increases dopamine concentration in the
synaptic cleft. This accelerates the binding rate for dopamine at D1 and
D2 receptors, while reducing it for D3 receptors in the mesolimbic
reward system (see Almey et al. 2015).
Ultrastructural analyses of estrogen receptors within dopamine terminal
regions such as the medial prefrontal cortex identified such receptors
in extranuclear sites of neurons and glia; the highest densities were
recorded at axons and terminals (Almey et al. 2014).
The
described neuro-circuitry of the reward system, which includes the
interplay between the dopaminergic system and estrogen, also plays a
significant role in female decision making. In one study of rats,
females were tested using an effort-discounting task with different
types of reward: pressing a lever once yielded two pellets, pressing it
many more times yielded four pellets. The results showed that
ovariectomized females expressed a preference for the high-reward lever,
whereas females treated with estradiol selected the low-reward lever.
Moreover, the application of ERα receptor agonists, independently of ERβ
agonists, resulted in high reward/high cost preferences, but
simultaneous application of agonists for both receptor types decreased
the choice for such high benefit/high cost options (Uban et al. 2012).
In
addition to the dopaminergic system, it is important to consider also
estrogen effects on the serotonergic brain system in relation to female
sexual behavior. Introducing ovarian hormones into the dorsal raphe
nuclei region of macaque brains altered the mRNA expression rates of
components involved in serotonin metabolism (Pecins-Thompson et al. 1998).
The rhombencephalic raphe nuclei complex is the origin of the
serotonergic system. From here serotonergic fibers project into almost
all brain areas (Holloway et al. 1993).
Lower brain serotonin concentrations are related, for example, to
depression, anxiety, and impaired cognition (Wallner and Machatschke 2009).
Application of estrogen with or without progesterone increased
tryptophan hydroxylase-I mRNA, but decreased mRNAs of MOA-A and
concentrations of the serotonin re-uptake transporter. The latter
impairs the relocation of serotonin metabolites from the postsynaptic
membrane into presynaptic regions. All of these manipulations affect
central serotonergic function (Smith et al. 2004), and serotonergic pathways are known to influence fluctuations in female mood and behavior during the menstrual cycle.
From
neurophysiological research we conclude that the actions of estrogen
and its related receptor system in the brain influence female behavior
in a socio-sexual context. The distribution rate and density of receptor
fields in subcortical brain areas enable estrogens to exert a major
influence on female sexuality, food intake, mood changes, feelings of
pleasure, and cognitive function in different phase of the cycles, in
which estrogen concentrations vary significantly.
Conclusion
Women
share with nonhuman primates subcortical brain areas, which are
essential to modulate behavioral and physiological changes in relation
to different reproductive cycle stages. These homologous regions
represent evolutionarily conserved structures documented in nearly all
vertebrates. The interconnected social behavior network and the
mesolimbic reward system are responsible for a basic integration of
sexual behavior and its related reward sensations. These sensations are
not limited to sexuality, but also include food intake (Adam and Epel 2007) and prosocial interactions (Rilling 2011).
Here, emotional rewards are produced mainly via the dopaminergic
system. Research on rhesus macaques has revealed two types of dopamine
neurons, one excited by reward-predicting stimuli and the other
inhibited by punishment-predicting stimuli (in this case, an airpuff).
Importantly, more neurons are excited by both stimuli combined
(Matsumoto and Hikosaka 2009).
These results indicate that the dopamine system can differentiate
between positive and negative signals. Matsumoto and Hikosaka (2009)
proposed the existence of two functionally distinct dopamine neurons,
the airpuff-inhibited and the airpuff-excited type. They would be
located in subcortical brain areas belonging to the mesolimbic reward
system. In mammals, the mesolimbic reward system and other dopaminergic
systems project to the prefrontal cortex, but the innervation density of
the cortical striatum differs between humans and nonhuman primates
(Raghanti et al. 2008).
Moreover, the distribution of estradiol receptors in subcortical
(Gonzales et al., 2007) and cortical areas suggests that value-oriented
signals can be transformed into distinctive behaviors modulated by
estradiol concentrations during different cycle phases. Such hormonal
modulations are apparently homologous and stable in physiological and
behavioral expression rates across species (Uban et al. 2012).
Regardless of differences in the ways in which some primate species
advertise or conceal ovulation, there may still be functional
similarities in the way sexual stimuli are perceived, processed, and
communicated. One important difference between humans and other primates
may concern women’s strategic behavioral decisions in relation to their
fertility. Women have to make sure that the prospective fathers of
their children are able and willing to invest significant resources in
themselves and their children to an extent that is rarely observed in
nonhuman primates.
Pair-bonding mechanisms
have evolved in humans to make possible cooperative investment in
children between reproducing partners. Such social bonds, however,
should not be confused with sexual monogamy. The earliest primate
ancestors may have had a solitary lifestyle similar to that of nocturnal
mammals. Their descendants adopted a multi-male, multi-female social
system approximately 52 million years ago, and subsequently evolved
pair-living and one-male groups (harems) approximately 16 million years
ago. Across all primates, monogamy is a less frequent social system than
harems or multi-male, multi-female societies (Shulez et al. 2011).
Nonetheless, social bonding between the sexes is probably tighter in
one-male units than in multi-male, multi-female groups. At the level of
mechanisms, these bonds are mediated by the neuropeptides oxytocin and
vasopressin, which are produced in the magnocellular neurons of the
paraventricular and supraoptic nuclei of the hypothalamus. These neurons
project into areas of the mesolimbic reward system, such as amygdala or
hippocampus, and into regions of the social behavior network, such as
the BNST or the POA (Meyer-Lindenberg et al. 2011).
The projections into these subcortical brain areas suggest that social
bonding mechanisms may be related to sexual activities, and in
particular to their emotional positive rewards (Young and Wang 2004).
Both brain areas are evolutionarily relatively old. Therefore, we
suggest that the neural circuits regulating sex – its emotional positive
reward in relation to pair-bonding - were established after the
evolution of single-male units in humans and nonhuman primates. This
means that the origin of advertising female sexually attractive signals
is older and originated in multi-male, multi-female primate societies.
Women’s
pre-fertilization selection process for socially compatible and
genetically valuable partners with high status and resources is
time-consuming and subject to female-female mating competition. Women’s
fat reserves, which are needed for succesful ovulation, gestation, and
lactation, can contribute to permanent signals of sexual attractivenss
such as large breasts and buttocks, which may signal physical and
genetic fitness. Such permanent sexual signaling may allow females
lengthier periods of mate assessment and more opportunities for mate
choice without losing the interest of prospective partners. Studies have
shown that men find attractive particular values of the waist-to-hip
ratio as well as of the body mass index, which signals general health
(Singh 2002; see also Havlíček et al. 2015
and commentaries). Additionally, breast morphology and size in fertile
females may enhance the sexual attractiveness of the so-called hourglass
body shape in women (see Dixson 2009).
A question may arise as to whether men can perceive changes in female
SSC in relation to culture-specific norms such as using different
clothing during different cycle phases. For example (see also 2.4), the
water content and parenchymal tissue volume increase in women during the
luteal period and decreases during menstruation. As wearing clothes is
common in most human societies, men are probably unable to recognize
subtle cyclic changes in women’s bodies when these are covered by
clothes. It is also unclear whether men can detect changes the bodies of
women with whom they are in permanent, stable relationships. Male
perception and interpretation of the information content of female SSC
may result from direct comparison of their shape and size between women,
independent of their cycle stage. Such individual differences may
provide information about a woman’s health or reproductive fitness. In
this context the American College of Radiology classified different
mammographic density stages based on the fat-to-parenchymal tissue
content in relation to the risk of developing cancer. Overall, a higher
proportion of parenchymal tissue compared to fat is related to cancer
(type 1, ≤ 25% of parenchymal tissue; type 2, ≤ 50%; type 3, ≤ 75%; type
4, ≥ 75% parenchymal tissue). This classification shows that the ratio
can vary extremely. Therefore, the fat content of female SSC
communicates information about health and energy resources available for
reproduction and parental investment. But the attractiveness in
particular breast sizes and/or shapes is not necessarily a fitness
marker insofar as a significantly reduced fat proportion is related to
less available energy resources and to increased health risks (see
above). In this context, more subtle changes in other body parts during
the cycle - the lipid content of the skin, the fat content of the thighs
and abdomen, pigmentations, etc. – would provide significant
information but they are presumably not reliably detectable by men, even
those living in long-term partnerships.
Importantly,
women do change their behavior in relation to cycle phases. Some of
these changes are obviously linked to their culture. During
periovulatory periods, women advertise their fertility not only by
changing their gait, but also by wearing particular clothes and make-up;
their consumer behavior and food consumption are also different.
Advertising fertility through make-up or clothes would be analogous to
cyclic changes in sexual swellings or face coloration in nonhuman
primate females. Functionally, both the morphological changes in
nonhuman primates and the behavioral strategies in humans are caused by
female intra-sexual competition for valuable mates and by male mate
choice. Interestingly, neither the morphological changes described in
nonhuman primates nor the culture-specific behaviors of women seem to
reliably signal fertility, ovulation, or readiness to mate: exaggerated
swellings are also expressed during non-fertile cycle phases and sexy
clothes can be worn by women in all phases of the cycle. Possibly, the
culturally developed use of specific clothes to enhance and accentuate
sexually attractive body areas in women can be interpreted as an example
of culture – biology co-adaptation that better highlights permanently
attractive SSC under competitive partner market conditions (Puts 2010).
If
the female SSC of nonhuman primates and humans do not directly inform
males about females’ fertility, − they might, in some cases, signal
females’ genetic fitness and physical condition. For example, wearing
particular clothes may allow women to make some of their attractive
bodily characteristics, such as a thin waist and wide hips, more visible
to men. Since women’s preferences for clothes and men’s preferences for
body shapes are known to be different in relation to cultures and
historical periods, a full understanding of female sexual signaling and
male responses to it in humans requires the integration of biological
and cultural analyses.