Female dominance in spotted-hyenas (Crocuta crocuta) and other similar systems: implications for understanding human sexuality

by Farah Kabir

Abstract

Sexuality is a topic that social theorists have debated for years, but they have yet to develop a solidifying definition. The differentiation between what has been considered normative male and female sexual behavior remains unclear when we consider individuals who exhibit qualities that defy the dichotomizing physiological and behavioral distinctions instilled in human society. Here, I review one such atypical system in which females play the typical male role in a society. The spotted hyena (Crocuta crocuta), native to Sub-Saharan Africa, exhibits female dominance behavior as well as male-typical morphological characteristics, such as a pseudo-penis. I will highlight the reproductive endocrine regulation of the female spotted hyena reproduction to help elucidate a possible mechanism regulating female dominance and other behaviors in this species. Additionally, I will compare certain endocrine mechanisms and behaviors of the spotted hyena to other female dominated systems, including those of the ring-tailed lemur (Lemur catta), rock hyrax (Procavia capensis), and callitrichine primates. Broader implications of these findings can help us better understand the continuum of sexuality in women in order to elucidate social implications of how humans distinguish sex, sexuality, and associated behaviors.

Introduction

Simone de Beauvoir’s groundbreaking work The Second Sex transformed perceptions of human sex dynamics by rejecting biological differences as the basis for social practices. She stated that females are perceived to be biologically inferior to males and incomplete because they lack an organ: the penis. Furthermore, she assesses that females are subordinate to males because hormonal differences allow males greater muscular strength and respiratory capacity (Beauvoir, 1953). However, these maleness-determining criteria are inadequate when we consider spotted hyenas. Female spotted hyenas possess an extended penis-like clitoris and are socially dominant over breeding adult males in their group. Furthermore, the reproductive endocrinology of atypical female mammals such as ring-tailed lemurs, rock hyraxes and callitrichine primates reveal that males and females have similar androgen levels as males. Not only does this finding challenge the classical role of androgens as masculinizing hormones, but also it suggests the presence of androgen-independent factors that influence the observed sex-role reversal in these animals in the wild. Investigating these factors will foster a better understanding of the relationship of the physiological and behavioral nature of sex dynamics as well as current understanding of the social implications of sex distinction.

Female urogenital system and search for source of “masculinized” external genitalia

In Lessons from the Intersexed, Suzanna J. Kessler exposes the tendencies of physicians in the late 20th Century to assign sex to newborns with ambiguous genitalia based on the size, shape, and location and the insistence on clitorectomy when faced with enlarged clitorises that are simply deemed unnatural. This method of sex differentiation is inadequate when we consider the female spotted hyena. Female spotted hyenas have dramatically masculinized external genitalia including an elongated hypertrophied clitoris that resembles the male penis. In addition, the resemblance of their fused vaginal labia to male physiology led to the terminology pseud-scrotum. A urogenital sinus, where the urethra joins the reproductive tract, traverses this pseudo-penis. (Cunha et al, 2003) This enables hyenas to urinate through their pseudo-penis just as males do. Lacking an external vagina, the female spotted hyena’s vagina is located internally inside the abdomen-pelvic cavity. (Cunha et al, 2003)

Despite the similarities in appearance and some function, there are external and internal morphological differences between male and female genitalia. Although they appear similar in size and shape in the flaccid condition, the male penis and female pseudo-penis exhibit prominent differences in the erectile condition. For instance, the glans clitoris of females tip appears rounder, while the glans penis of males appears more angular. The erectile male penis is also more flexible than female pseudo-penis, which allows males to better achieve successful mating (Cunha et al, 2014). Furthermore, not only is the female pseudo-penis able to receive the male penis during copulation, but also it functions as a birth canal. Females are able to give birth to one or two infants through their pseudo-penises. Unlike males, females display erections in the context of ceremonial greetings rather than sexual contact (Frank et al, 1990). Although they lack external vaginal openings, females retain ovaries, oviducts, uteruses, and upper vagina common to other female carnivores. (Cunha et al, 2003)

Role of androgen mediation of genital “masculinization”

As the masculinized features in female hyenas are present at birth, many researchers have looked to fetal development to understand the mechanisms behind the formation of the spotted hyena’s unique urogenital anatomy and sex differentiation (Glickman et al, 2006). The contemporary basis of sexual differentiation originates from the Jost Model. In the 1940–50s Alfred Jost asserted that during an initial crucial stage in development, fetal testes secretion of androgens produced masculine urogenital phenotype, while the secretion of anti-Mullerian hormones lead to regression of the Mullerian ducts. The secretion of these hormones would lead to the development of testes, while their absence would lead to the formation of the female urogenital system and ovaries. (Jost, 1972)

Application of this model revealed that exogenous androgen treatment on fetuses during crucial development stages produced masculinized external genitalia. (Licht et al, 1998) Thus, scientists extended this model to the spotted hyena and began searching for the source of circulating androgens, which they believed would account for the female pseudo-penis. The pseudo-penis’ lack of follicles and extra interstitial tissues made female ovaries a possible source of androgens. (Mathews, 1939) However, the development of female urogenital system before differentiation of fetal ovary and adrenals eliminated ovaries as the source (Licht et al, 1998).

Drea (2007) showed higher levels of androstenedione AE, which can be converted into either testosterone (T) or estrogen, were found in female hyenas with 90% of AE originating from the ovaries. Based on the high 17 B-hydroxy-hydrogenase, an enzyme that converts AE to T, activity in the placenta indicates that AE may be the source of increased T levels passed on to developing fetuses of either sex. Anti-androgen treatment on pregnant females complicated this theory further. Anti-androgen treatments involved the use of flutamide, an androgen receptor blocker, and finasteride, an inhibitor of T conversion to dihydrotestosterone. Rather than observing external genitalia common to more traditional female mammals, the treated mothers gave birth to females that retained both pseudo-penises and pseudo-scrotums. However, there were some functional differences in morphology and endocrinology in these females. For instance, the size and elasticity of the urogenital meatus increased, while the clitoral length decreased. Also, they exhibited elevated plasma estrogen concentrations and increased glans diameter in adult females. Overall, female clitorises resembled those of traditional female mammals as they were shorter and thicker (Cunha et al, 2005).

Furthermore, they found that while both sexes received androgens via placental transfer in early stages of development, males are supplemented with androgens from fetal testes during critical stage in urogenital development. Males born to anti-androgen treated mothers also experienced “feminizing” characters. In addition, the male penis resembles the morphological characteristics of females both externally and internally. Males were born with short penises that prevented reproductive success as adults, because stunted penises were unable to physically penetrate and maintain entry into female clitorises. Also, male penises were thicker and had a rounded rather than angular glans (Drea et al, 1998). The internal structure of the penis became “feminized” as anti-androgen males displayed larger urogenital systems common in females. Males lost the corpus spongiosum and retractor muscles, the prostate gland, which were features specific to males. The bulbocavernosus muscles also appeared similar to those of females (Cunha, 2005). Thus, the conservation of “masculinized” features and display of more “feminized” characteristics reveal that androgens do potentially influence the morphology of unique external genitalia of female spotted hyenas.

Separate hierarchies and female dominance

In addition to masculinized external genitalia of females, the sex-role reversed social structure of spotted hyenas and female dominance make these atypical mammals deviate from traditional mammalian patterns. Spotted hyenas are social mammals originating from sub-Saharan Africa that live in intersex clans in fusion-fission societies that follow separate and stable social ranking hierarchies. In these fission-fusion societies clan members live in solidarity but often form small groups. Each clan defends group territory and females raise their cubs in a communal den (Goymann et al, 2003). During periods of low prey, all Serengeti females will leave clan territory in search of distant migratory prey regardless of social status. On the other hand, females with higher social status monopolize “low-cost foraging options” (East and Hofer, 2002) during periods of medium-prey, while those with lower status must invest more energy into travelling in order to find migratory prey. Thus, high ranked females are able to invest more energy nursing their cubs. Subsequently, cub growth rate becomes dependent on female social status as cubs of high-ranked mothers grow faster, reproduce earlier, and live longer (East and Hofer, 2002).

While, all females inherit the social rank of their mothers, males acquire their rank differently depending on their dispersal status. Natal adult males, those born to the clan, and immigrant males, those that have dispersed from other clans, follow separate mechanisms of social ranking that neither depend on fighting ability or physical size (Dloniak et al, 2004). Social rank of dispersal or mating natal adult males, who are around two years old, is similar to females in that they inherit the social rank of their mothers. While cubs with high-ranking mothers tend to get more support with maintaining their status, cubs with lower-ranked mothers are not as lucky (Engh et al, 2000). Unlike these natal hyenas, immigrant adult males are capable of advancing their social rank based on a queuing rank system. The death or emigration of a male ranked above them provides an opportunity to climb the dominance hierarchy (Dloniak et al, 2006). Unlike males, female spotted hyenas remain within the clan they were born into for life (Goymann et al, 2001).

Although adult males and adult females have separate dominance hierarchies, females exhibit absolute dominance to adult males in every social situation. This dominance is exhibited by immigrant male-female relationships in clans that are dictated by social status and tenure. Immigrant males with higher social status and longer tenure behave increasingly friendly towards females and in return, high rank females are more tolerant of them than recent immigrants. Furthermore, females that observe higher social status than another females will also exhibit ritualized greeting ceremonies, in which socially subordinate females will show signs of submission towards dominant females (East and Hofer, 2002). Thus, not only do female spotted hyenas display more “masculinized” physiological features, but also they exhibit “masculinized” behavior typical of males, which suggests there is a link mediating the physiological and behavioral characteristics.

Role of androgen mediation of female aggression and social dominance

Several studies have related feminine androgenization in utero of female spotted hyenas to female dominance and aggressiveness. Dloniak et al (2004) showed that females are exposed to unusually high levels of androgens during development, weigh more than males, and act more aggressive than adult males. Previously, prenatal exposure to high levels of androgens was believed to be the source of masculinization of female cubs. Both males and females exposed to higher levels of androgens during the second half of gestation were found to exhibit higher levels of aggression compared to those exposed to lower levels. This is consistent with previously findings that have established a positive correlation between androgens and increased rates of aggression (Engelhardt et al, 2000). Furthermore, modern understanding of sexual differentiation uses androgen circulation to female fetuses to explain the development of male-like genitalia. Although Goymann et al (2001) did not determine a positive relationship between male social rank and androgens extracted from blood samples, the authors found that males had higher androgen levels when exhibiting reproductive aggression. This study along with many others indicate a close tie between aggression and dominance in male mammals, which suggests that androgens may also play a role in female aggression and dominance as organizing hormones during fetal development or activating hormones during adulthood. Baker (1990) showed that anti-androgen treated mothers’ cubs and juvenile females that have undergone ovariectomies exhibited less aggression. Regardless of whether the effects are direct or not, these findings reveal that androgens clearly play a role in female aggression in spotted hyenas.

However, in contrast to these findings, a study by Drea et al (1998) showed that prenatal androgen exposure is not related to intrasexual aggression among females. These results suggest the link between androgen levels and variation in aggression in both females and males may not be so concrete (Drea et al 1998 and Dloniak et al, 2006). Goymann et al (2001) conducted a study in the Serengeti National Park in northwestern Tanzania, East Africa. They found that total levels of circulating androgens in adult females were less than postdispersal (breeding) adult males. Specifically, there were lower levels of T in females than males, while no significant difference in AE levels were found. Dloniak et al (2004) showed that pregnant females had higher fecal androgen levels than lactating females. They also found that T levels in female spotted hyenas were not significantly greater and fell within the T level range of other female carnivores, such as brown hyenas (Hyaena brunnea), striped hyenas (Hyaena hyaena), wolves, and domesticated dogs as well as the T range for female primates such as baboons (Simia hamadryas), chimpanzees (Pan troglodytes) and humans. Together, these findings suggest that females follow standard mammalian androgen trends and that higher androgen levels are not a selective factor to female domination in spotted hyenas. In the same study, Dloniak et al (2004) also found that predispersal males had lower T levels than postdispersal males even though predispersal males dominate postdispersal males, have higher hourly rates of aggression, and win all agnostic interactions with postdispersal males. These finding are unusual because in many other species, higher T levels are usually associated with more aggressive individuals and “winners” of competitions (Goymann et al, 2001).

Another type of aggression believed to be a by-product of androgenization is siblicide. Siblicide, or death resulting from sibling rivalry, has been observed as either obligate or facultative in mammals. The latter occurs when resources are limited, while the former is resource-independent. Thus, previous studies asserting that spotted hyenas exhibited obligate siblicide turned to androgens to explain why sibling rivalry within litters of same-sex cubs culminates to death. It has been posited that siblicide allows selection for large, aggressive female spotted hyenas that would dominate males. However, later studies observed that the frequency of twin litters positively correlated to the amount of resources; there were greater occurrences of all-female litters in well-fed clans. Thus, sibling rivalry occurred when mother’s milk supply was limited and involved dominant cubs restricting access to mother’s teat and the subordinate cubs eventually dying from starvation. However, facultative-resource based siblicide exhibited a sex-bias with respect to sex composition of twin litters, which suggests that there may be an unequal maternal investment in female cubs. (East and Hofer, 2002) Thus, while androgens may play an organizing role in development, it is unclear whether they play an activating one in adults that explain aggressive behavior. Furthermore, aggression and dominance may be driven by androgen-independent mechanisms.

Androgen- independent explanations for female aggression and dominance

Androgen-independent mechanisms that may be involved in the evolution of sex-reversed traits of spotted hyenas include female reproductive physiology and social dominance, decreased male aggression. These mechanisms may also explain the subordination of postdispersal males to postdispersal natal male spotted hyenas. Furthermore, a study by Glickman et al (2005) proposed that the social organization of spotted hyenas is a greater determinant of female dominance than organizing androgens, which suggests that social dominance may not be a product of hormone levels. However, a study by Dloniak et al (2006) offered that social and behavioral mechanisms of female dominance are not driven, but associated with androgens. Although interactions with dominant females did not produce direct androgen level variation in adult males, a relationship between high fecal androgen levels in immigrant males and the degree of association with attractive females, those that are close to conception, was found instead (Dloniak et al, 2006). This finding indicates that there potentially might be an endocrine response in males in close association with cycling females that helps synchronize the physiological and reproductive behavior between immigrant males and females.

Furthermore, Dloniak et al (2006) suggested that in order to properly investigate the relation between aggression and other factors it is essential to socially contextualize it. Aggression is typically classified based on the following behaviors: lunging, biting, chasing, displacing, pushing, and standing over with intention to bite. Dloniak et al (2006) further contextualized this behavior in terms of reproductive versus non-reproductive aggression. These authors assessed aggression between males that are within 10 meters of a female constitutes as reproductive aggression and aggression between males not in the context of a female constitutes as non-reproductive aggression. Furthermore, courtship behavior was defined by presentation, bowing display pawing the ground, mounting, and an approach/avoid display. They found that reproductive aggression and courtship behavior were good predictors of increased fecal androgen levels in adult immigrant males. However, they noticed that the relationship between male interactions with females and increased fecal androgen levels was independent of defensive aggression between males. Like females, males rarely directed reproductive aggression towards other males. When they did exhibit aggression it consisted of low-level threats. Specifically higher ranked males would protect higher ranked females against lower ranked males that were harassing them. Thus, aggression cannot simply be assessed based on direct effects of hormonal levels; rather, the social context must be analyzed in order to understand how reproductive endocrinology of spotted hyenas relates to their behavior.

Problems with inconsistent findings due to lack of standardized methodology?

Much variation appears to exist concerning strategies implemented to measure androgen levels in wild female mammals. Earlier researchers obtained blood samples using varying blood collecting protocols. In addition, the process of immobilization not only limited sample sizes but also may have influenced the results of the assays. The invasive nature of darting each wild hyena may have caused additional stress. More recently, a study by Dloniak et al (2004) suggested a non-invasive method of obtaining samples from fecal samples. Alternative sources of samples used for non-invasive measurements of androgens in other mammals include saliva, urine, hair and milk. However, this form of measurement has issues as well. Firstly, the clearance rate, or how long the steroids remain in the plasma, varies according to the sample source. For example, fecal sample clearance rate is in order of hours-to-days while that of saliva is in order of minutes. Secondly, the hormones measured in excretion may differ from hormones that actually act on the target organ due to steroid metabolism from secretion to excretion. Therefore, it becomes necessary to identify the chemical structure of the hormone of interest. (French et al, 2013)

Furthermore, the varying methods of extracting and assaying the samples could potentially add to issues with data interpretation. Experimenters use immune-based quantitative assays with antibodies with varying degrees of specificity to target androgens. High specificity allows for low-cross reactivity and reassurance of accurate quantitative measurements for a specific steroid concentration, while low specificity allows for high cross-reactivity and identification of multiple steroid concentrations. While the former allows the observation of a specific steroid on behavioral outputs, the latter enables analysis of a bigger picture of not only the steroid of interest but also of biological precursors and active downstream metabolites. Thus, it becomes essential to consider the level of specificity desired when conducting research. (French et al, 2013) Another issue unaddressed by some studies is the reproductive status of individuals such as predispersal versus dispersal males and pregnant, lactating, or nonbreeding females. (Goymann et al, 2001) These are important distinctions to consider when examining such physiological variables, because different biological states can alter hormones of interest.

“Masculinized” physiology and behavior in other atypical mammals

Although males typically exhibit higher T levels, aggression, and dominance than females in most mammals, there are several examples besides the spotted hyena that exhibit female dominance. It is important to study these other systems to gain a broader understanding of what appear to be conserved mechanisms of female dominance behavior. Furthermore, these findings can potentially provide broader implications for the evolution of human systems of dominance.

Female ring-tailed lemurs are a species of strepsirrhine primate from Madagascar that share morphological and behavioral similarities to female spotted hyenas. First, both display genitalia that resemble that of their male counterparts; female lemurs have enlarged and elongated clitorises with similar placement of urinary meatus as males (Drea, 2007). Second, pregnant female ring-tailed lemurs show increasing androgen levels that peak in the third trimester similar to spotted hyenas — although not as high—-which also exhibit higher androgen levels in late gestation. Specifically, females pregnant with female fetuses exhibited higher androgen levels of AE, T and E2 than preconception and postpartum values also peaking in the third trimester during organizational periods of time associated with external genitalia differentiation as well as neural substrates associated with behavior (Drea, 2011). Third, female lemurs practice reproductive control, which lends to advantages like priority of access to resources (Drea, 2007). These data suggest that there may be a relationship between androgens and both morphological and behavioral characteristics of female social dominance.

However, while spotted hyenas breed year round, ring-tailed lemurs breed seasonally, which suggests seasonal variation of sex steroids and aggression may exist. Thus, although adult males exhibit higher T levels than adult females in both spotted hyenas and ring-tailed lemurs, it might not be valuable to compare these findings due to differing breeding patterns. Regardless, these similar T levels, which fall into the range of typical female mammals that do not show masculinized morphological or behavioral features, imply that androgens may not be the determinant of male-like genitalia and female social dominance in ring-tailed lemurs. Furthermore, it is unclear whether female social dominance in ring-tailed lemur is determined by an androgenic or estrogenic mechanism as high levels of both AE and estradiol (E2) were found in females during the breeding season (Drea, 2006).

The rock hyrax, an African social mammal, is another example of a mammal where the females are on average more dominant than males and resemble the behavior and physiology of spotted hyena. Rock hyraxes live in mixed-sex groups in which females participate in cooperative rearing and most agnostic behavior, such as threat displays, chases, and avoidance occurs between males and females rather than intrasexually. Females assert their dominance by claiming sitting site priority and winning aggressive interactions. Just like spotted hyenas, both male and female rock hyraxes show similar T levels, which initially suggested that T played an activating role in female aggression (Koren et al 2006). However, a study by Koren et al (2006) on rock hyraxes, located in the Ein Gedi Nature Reserve, west of the Dead Sea in Judean Desert, Israel, discovered that T levels were independent from individual aggression rates and dominance that varied among females. Thus, this variation among individual females further suggests that T and female aggression are not related. Another similarity between rock hyraxes and spotted hyenas is intrasexual androgen variation. Just as postdispersal adult male spotted hyenas show lower T levels than presdispersal adult males, dominant female rock hyraxes exhibit lower T levels than subordinate females (Koren et al, 2009). This supports the idea that androgen-independent mechanisms are involved in female aggression and dominance. However, it may also suggest that high androgen levels may actually be a disadvantage to either males and females or spotted hyenas and rock hyraxes as high androgen levels are associated with lower social rank. On the other hand, while female and male rock hyraxes have similar T levels like spotted hyenas, they vary between lower ranking males and females where females have higher T levels.

It is important to note that Koren et al (2009) collected fur samples to assess T levels, while spotted hyena T levels were assayed from blood samples and fecal matter. Another factor to consider is that rock hyraxes are seasonal breeders like ring-tailed lemurs; females give birth in the spring. Koren and Geffen (2009) suggest temporal changes in androgens in males are the result of trade-offs between parental care required of reproductive success and aggressiveness required to maintain social rank. Thus, the methodology used to study behavioral endocrinology of rock hyraxes and that of spotted hyenas may influence how female dominance is compared and analyzed across species.

Regardless of their differences, both female rock hyraxes and spotted hyenas show levels of androgens that are as high as males—-something not commonly seen in most mammals where males are dominant and show higher androgen levels. Koren et al (2009) found a negative correlation between female social status and the androgens T and AE. This leads to the question of the possible impact of androgens on female fecundity in vertebrates. Browne et al (2006) showed that androgens could possibly delay female reproduction and embryo implantation in female northern fur seals. Furthermore, the cost of maintaining high androgen levels may interfere with reproductive costs. High androgen costs include: high energetic demands, reduced fat storage, interference with paternal care, impairment of immune system, increased risk of injury from greater activity and possibly aggression (Glickman et al, 2006). Reproductive costs include: reproductive energetic reserves and development of maternal behavior. Surprisingly, Koren et al (2009) found a negative correlation between female social status and the androgens T and AE, which suggests that female rock hyraxes were able to circumvent the reproductive interference of T. A study by Wingfield et al (2001) on T cost avoidance offered some possibilities as to how this could happen. For one, high androgen levels could be avoided via hormone-binding proteins. Second, the rock hyraxes could have acquired sensitivity to behavioral effects of androgen via downregulation of receptors and enzymes. These possibilities represent mechanisms that have evolved in female mammalian species to cope with high androgen levels and increase fitness.

Callitrichine primates, specifically marmosets and tamarins are another example of mammals that exhibit female dominance. Female dominance and aggression is generally assessed by food competition and territorial behaviors. These primates show less intragroup aggression and more intergroup aggression; females will display non-contact aggression and display threats towards other females (Lazzaro et al, 2001). Uniquely, marmosets and tamarins usually give birth to fraternal twins and are exposed to high concentrations of androgens that influence morphological and behavioral development. Unlike female spotted hyenas, marmoset fetus exposure to high androgen levels at late gestation was associated with a decreased display in juvenile aggressive behavior. This manifested in the form of rough-and-tumble play in females but more aggressive behavior in males. Thus, prenatal exposure to androgens varies in marmosets and spotted hyenas, two species that both exhibit female dominance. A study on postnatal exposure to androgens in tamarins revealed that females treated with T for the first 50 days of postnatal life exhibited greater rough-and-tumble play as juveniles. Various outside factors, including postnatal steroid environment and social influences such as the sex of play partners, may explain this finding.

Evolutionary costs and benefits of sex-reversed traits in atypical mammals

Although the pseudo-penis in female spotted hyenas may be a symbol of female dominance, the organ poses many challenges to survival and fitness. The placement of urogenital meatus or reproductive tract opening through the pseudo-penis allows a pregnant female to give birth that is not only time-consuming but also destructive. The short umbilical cord characteristic of spotted hyena fetuses requires the fetal-placental unit to detach from the uterus early on during the birthing process. This condition can potentially lead to a stillbirth by oxygen depletion if the fetus remains in the pseudo-penis for too long. Furthermore, rupture at the caudal side of the organ during delivery leaves the mother with a large bleeding wound, a source of infection (Goymann et al, 2006). A study by Glickman et al (2005) on captive hyenas observed that pregnant females in their colony produced 60% stillbirths. Moreover, the placement of the pseudo-penis in front of the hind legs and lack of erection during mating makes it difficult for males to identify the urogenital meatus. Males have been observed to squat so far down under the females that their rears are touching the ground in order to position their erect penises into females’ flaccid pseudo-penises. Finally, the non-sexual erectile characteristic of the pseudo-penis requires females to completely cooperate with males in order for complete copulation (East et al).

Theoretically, maintenance of this unique female organ should not be evolutionarily selected for considering all the mating challenges and fitness costs that lower reproductive success. Glickman et al (2005) observed that delivery was much easier for females birthed from anti-androgen treated mothers because of the features of their more “feminized” external genitalia. Easier births were more rapid, therefore low-risk compared to natural births of untreated females. Moreover, there were no deaths via parturition for these anti-androgen treated females. East et al (2002) proposed that the benefits of the pseudo-penis outweigh the costs. The problems posed by pseudo-penises can be interpreted as benefits, because they give females greater control over copulation. As success of mating relies fully on the extent of female participation, female spotted hyenas are allowed a great amount of mate selection. Thus, this may explain why male-male aggression frequency is low, because energetic costs of reproductive aggression in terms of male-male aggression are redirected as reproductive aggression to developing relationships to females and preventing males from approaching females.

Furthermore, the maternal rank inheritance may play a role in males investing more energy to form close relationships to females through shadowing and affiliative relationships rather than competing and fighting in order to ensure their own as well their offsprings’ ranks. Although lower ranked males did not shadow or defend them, they did concentrate their affiliative behavior on young adult females, while high ranked males additionally protected higher-ranked females (East and Hofer, 2001). Similar to males, lactating female mothers do not frequently engage in fighting or aggressive behavior against one another. In the context of the communal den, the most benefit from aggression higher-ranked females can show is denying lower ranks access to den areas. On the other hand, the benefits associated with mid-rank and lower-rank females exhibiting affiliative behavior with other females of higher rank that may outweigh the costs of female-female aggression. Firstly, there is a reduced risk of facing social harassment from dominant females. Secondly, affiliation increases the chance of securing support from these dominate females. Lastly, affiliation increases tolerance of dominant females to those of lower ranking during feeding on large kills (White, 2007).

Testosterone and aggression in women

Dual-hormone hypothesis

While the link between T and aggression has been shown in males of various species in many studies, the role of T in female aggression remains less understood. Conflicting results among past research has led researchers to consider the dual-hormone hypothesis, which claims that the stress hormone, cortisol (C) moderates T’s effect on aggression. (Denson et al, 2013) This hypothesis is based on the idea that T is positively related to aggression only when C concentrations are low. One explanation for the interaction between T and C is that the former inhibits the HPG axis and the latter inhibits the HPA axis. Another possible explanation is that behavior mediates C’s influence on T. C causes behavioral inhibition rather than physiological inhibition of T synthesis or activation (Densen et al, 2013).

Past studies that support the relationship between low C and high T focused on male aggression reported in clinical populations, which included adolescent offenders, psychopathic individuals, and adolescents with conduct disorders. Geniole et al (2011) conducted a study with undergraduate men suggesting that T-C interaction was an indicator of triggered aggression. This aggressive behavior was often evoked as a response to some kind of social provocation. The provocation came in the form of social exclusion or inclusion during a ball-toss game against two other simulated players. This was followed by an aggression task in which the participant was allowed to periodically take money from the other players. This progressed when the other fake players were able to periodically take money from the participant. The authors observed that there was generally more aggression seen in participants that were included rather than excluded, and that there was a positive correlation between participants being socially included and their enjoyment of the tasks. Furthermore, data patterns indicated T concentrations tended to be high, while C concentrations were low when participants were socially included and vice versa for excluded participants (Geniole et al, 2011).

Using this research as a basis, Denson et al (2013) investigated whether endogenous T-C interaction could be an indicator for heightened female aggression by examining aggressive behavior in the context of social competition. It has been previously shown that winners often exhibit higher levels of T concentration than losers based on a feedback loop mechanism between an organism’s T level and it’s assertiveness to win the competition. Furthermore, research with rats has shown that competitiveness increases after winning in order to claim even higher status. On the other hand, research has shown that losing in humans can decrease T levels and inhibit them from competing in future competitions. This has been observed not only in men, but also in women, particularly in a study by Oliviera et al (2009) on female badminton players. Encouraged by these findings, Denson et al (2013) conducted an experiment, which was disguised as a competitive reaction time task, on 60 female undergraduates from University of New South Wales. After a fake participant would intentionally insult her, a real participant was given the opportunity to retaliate during a 25 trial reaction time task. The reaction time task involved a competition testing how fast one could click a computer mouse as the color of a small box changed from yellow to red on a computer screen. Retaliation came in the form of white noise, which one could blast at her provokers from a range of 0–10 intensity, a scale used to measure level of aggression.

Hormone assays performed on saliva samples revealed that basal T levels were indicative of increased female aggression at high C levels. This contradicted past findings on males, which supported the dual-hormone hypothesis. Although the authors did not find a baseline for T-C interactions, it is possible that high C levels may cause hypersensitivity to socially threatening situations. Thus, the consistency of the Denson et al (2013) and Geniole et al (2011) studies may be due to the fact that both used of social provocation to stimulate aggression.

Ultimately, the contradicting findings between the Geniole et al (2011) and Denson et al (2003) study suggest that the role of the dual-hormone hypothesis in aggression is not unisexually applicable. However, the consistent role of social provocation in stimulating aggression in both studies suggests the role of androgen-independent factors in aggression of both males and females. This supports previous conclusions drawn from spotted hyena research, which propose that social and behavioral mechanisms of female aggression and dominance are associated rather than directly correlated with androgens. Future research should focus on androgen-independent studies in order to achieve a greater understanding about sex-role reversal in the animal kingdom and its implications on evolutionary trends as well as implications on human sex determination and definition.

Hormone regulation in sports and implications for gender classification

Recently, T regulation in women’s sports has come to attention in light of events circling Indian national champion sprinter Dutee Chand’s expulsion from the Commonwealth Games, because she experiences hyperandrogenism, a condition that makes her bodies produce very high T levels. The International Association of Athletic Federations (IAAF) and International Olympic Committee (IOC) reasoned that Chand’s condition allowed her an unfair advantage to compete against female athletes. This decision has been the source of controversy as it highlights the problems with sex-determination and underrepresentation of intersex rights in international society. While Chand’s story is currently a heavily discussed topic, this is not the first time a situation like this has taken place. Female athletes who experience hyperandrogenism have been and continue to be encouraged to suppress their T levels by taking drugs or getting surgery to limit hormonal output (Macur, 2014). The issue with this type of response to female athletes like Chand is the invisible solicitation of the sex-differentiation rules instilled in society, which have less to do with biology and more to do with sociology. This evokes the fundamental question that feminists and social theorists have been asking for a long time: How do we define sexuality? Based on my review on female dominance systems in spotted hyenas and other atypical mammals, I believe that sex should not be determined by androgen levels, because research points to androgen-independent mechanisms of sex determination.

Throughout the history of human beings, men have generally been considered the “self” or the default human sex, while women have been considered “the Other” or “the deviation.” Furthermore, Simone de Beauvoir explains how people have rationalized patriarchal societies over time in the line: “Representation of the world, like the world itself, is the work of men; they describe it from their own point of view, which they confuse with the absolute truth.” (de Beauvoir, 1953). The existence and survival of sex-role reversal in atypical mammalian societies is evidence that patriarchal societies are not evolutionarily selected over all other forms of societies.

Conclusion

In this paper, the role of androgens in the development of “masculinized” physiology and behavior of several atypical female mammals has been explored. Females spotted hyenas stand as the species with the most dramatic exhibition of masculinity in the form of its pseudo-penis, pseudo-scrotum and absolute social dominance. Despite their ambiguous characteristics, none of the studies discussed in this paper discounted these unique mammals as females. Furthermore, the conclusion drawn from most studies was that female spotted hyenas do not express more T than males or even other more traditional mammals. In accordance with studies on atypical mammals, studies on women’s sports athletes also reveal that T levels are not definitive; they change depending on social and environmental circumstances, such as availability of resources, competition, pregnancy, and developmental stage. Moreover, while androgens like T play some kind of role in sexual characteristics, it is not yet completely apparent which characteristics are more important than others. Thus, it appears that there are no clear evolutionary conserved biological restraints that determine dominance in social organization of mammals. The existence of sex-role reversal in atypical mammalian societies reveals that while patriarchal societies have been prevalent throughout human history, they are not necessarily indicative of which sex is truly dominant.

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