Sex differences in otoacoustic emissions measured in rhesus monkeys (Macaca mulatta)

Click-evoked otoacoustic emissions (CEOAEs) and distortion-product OAEs (DPOAEs) were measured in about 60 rhesus monkeys. CEOAE strength was substantially greater in females than in males, just as in humans. DPOAE strength was generally slightly stronger in females, just as in humans. In males, CEOAEs were weaker (more masculine) in the fall breeding season and in winter than in the summer. In females, CEOAEs were slightly stronger (more feminine) in the fall, when sex steroids are elevated in females (and males), than in the summer when rhesus monkeys are reproductively quiescent. Thus, the sex differences in CEOAEs were greater in the fall than in the summer. We presume that the seasonal fluctuations in OAEs reflect activational hormonal effects, while the basic sex differences in OAEs likely reflect organizational effects of prenatal androgen exposure. Some monkeys of both sexes had been treated with additional testosterone or the anti-androgen flutamide during prenatal development. In accord with expectations, prenatal androgen treatment weakened CEOAEs in females, and prenatal flutamide treatment strengthened CEOAEs in males. For DPOAEs, the differences between treated and untreated groups were mostly small and often inconsistent. Taken as a whole, the data from both rhesus monkeys and humans suggest that the linear, reflection-based mechanism of OAE production that underlies CEOAEs is more sensitive to prenatal androgenic processes than is the nonlinear distortion mechanism that underlies DPOAEs.     

Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep (Ovis aries)

Otoacoustic emissions (OAEs) were measured in male and female Suffolk sheep (Ovis aries). Some sheep had been administered androgens or estrogens during prenatal development, some were gonadectomized after birth, and some were allowed to develop normally. As previously reported for spotted hyenas, gonadectomy did not alter the OAEs for either sex; accordingly, the untreated/intact and the untreated/gonadectomized animals were pooled to form the control groups. The click-evoked otoacoustic emissions (CEOAEs) exhibited by the female control group (N = 12) were slightly stronger (effect size = 0.42) than those in the male control group (N = 15), which is the same direction of effect reported for humans and rhesus monkeys. Females administered testosterone prenatally (N = 16) had substantially weaker (masculinized) CEOAEs than control females (effect size = 1.15). Both of these outcomes are in accord with the idea that prenatal exposure to androgens weakens the cochlear mechanisms that underlie the production of OAEs. The CEOAEs of males administered testosterone prenatally (N = 5) were not different from those of control males, an outcome also seen in similarly treated rhesus monkeys. Males administered dihydrotestosterone (DHT) prenatally (N = 3) had slightly stronger (hypo-masculinized) CEOAEs than control males. No spontaneous otoacoustic emissions (SOAEs) were found in any ears, a common finding in non-human species. To our knowledge, this is the first ruminant species measured for OAEs.     

Effects of prenatal treatment with antiandrogens on luteinizing hormone secretion and sex steroid concentrations in adult spotted hyenas,Crocuta crocuta

Prenatal androgen treatment can alter LH secretion in female offspring, often with adverse effects on ovulatory function. However, female spotted hyenas (Crocuta crocuta), renowned for their highly masculinized genitalia, are naturally exposed to high androgen levels in utero. To determine whether LH secretion in spotted hyenas is affected by prenatal androgens, we treated pregnant hyenas with antiandrogens (flutamide and finasteride). Later, adult offspring of the antiandrogen-treated (AA) mothers underwent a GnRH challenge to identify sex differences in the LH response and to assess the effects of prenatal antiandrogen treatment. We further considered the effects of blocking prenatal androgens on plasma sex steroid concentrations. To account for potential differences in the reproductive state of females, we suppressed endogenous hormone levels with a long-acting GnRH agonist (GnRHa) and then measured plasma androgens after an hCG challenge. Plasma concentrations of LH were sexually dimorphic in spotted hyenas, with females displaying higher levels than males. Prenatal antiandrogen treatment also significantly altered the LH response to GnRH. Plasma estradiol concentration was higher in AA-females, whereas testosterone and androstenedione levels tended to be lower. This trend toward lower androgen levels disappeared after GnRHa suppression and hCG challenge. In males, prenatal antiandrogen treatment had long-lasting effects on circulating androgens: AA-males had lower T levels than control males. The sex differences and effects of prenatal antiandrogens on LH secretion suggest that the anterior pituitary gland of the female spotted hyena is partially masculinized by the high androgen levels that normally occur during development, without adverse effects on ovulatory function.     

Otoacoustic emissions,auditory evoked potentials and self-reported gender in people affected by disorders of sex development (DSD)

Both otoacoustic emissions (OAEs) and auditory evoked potentials (AEPs) are sexually dimorphic, and both are believed to be influenced by prenatal androgen exposure. OAEs and AEPs were collected from people affected by 1 of 3 categories of disorders of sex development (DSD) — (1) women with complete androgen insensitivity syndrome (CAIS); (2) women with congenital adrenal hyperplasia (CAH); and (3) individuals with 46,XY DSD including prenatal androgen exposure who developed a male gender despite initial rearing as females (men with DSD). Gender identity (GI) and role (GR) were measured both retrospectively and at the time of study participation, using standardized questionnaires. The main objective of this study was to determine if patterns of OAEs and AEPs correlate with gender in people affected by DSD and in controls. A second objective was to assess if OAE and AEP patterns differed according to degrees of prenatal androgen exposure across groups. Control males, men with DSD, and women with CAH produced fewer spontaneous OAEs (SOAEs) – the male-typical pattern – than control females and women with CAIS. Additionally, the number of SOAEs produced correlated with gender development across all groups tested. Although some sex differences in AEPs were observed between control males and females, AEP measures did not correlate with gender development, nor did they vary according to degrees of prenatal androgen exposure, among people with DSD. Thus, OAEs, but not AEPs, may prove useful as bioassays for assessing early brain exposure to androgens and predicting gender development in people with DSD.     

The relationships between otoacoustic emissions and relative lengths of fingers and toes in humans

Both otoacoustic emissions (OAEs) and the relative length of the index and ring fingers (the 2D:4D ratio) exhibit large sex differences, and both exhibit masculinization effects in female homosexuals and bisexuals. Because these sex differences exist in young children, the implication is that both types of measure are affected by prenatal androgen exposure, but it has been unknown to what degree these two types of measure are related. Accordingly, OAEs and the relative lengths of the fingers and the toes were measured in 59 heterosexual females, 55 heterosexual males, 29 homosexual females, and 33 homosexual males. The correlations between the two types of measure were unexpectedly quite low in both the heterosexual and nonheterosexual groups. For example, the correlation between number of spontaneous OAEs per ear and 2D:4D was less than 0.25, for both sexes and both sexual orientations. One interpretation of these results is that the prenatal hormonal mechanisms producing the sex differences in OAEs differ in quality, degree, or timing from those producing the sex differences in relative finger length. That is, OAEs and 2D:4D may be windows onto slightly different prenatal processes or times during prenatal development. Measures of mental-rotation ability also were obtained on these participants, and those correlations with relative finger length also were small.     

Sex Differences in Territorial Behavior Exhibited by the Spotted Hyena (Hyaenidae, Crocuta crocuta)

Spotted hyenas ( Crocuta crocuta ) are gregarious carnivores that defend group territories against encroachment by neighboring conspecifics. Here we monitored the behavior of members of one clan of free-ranging spotted hyenas during border patrols, 'wars' with neighboring clans, and other interactions with alien intruders, to document differences between the sexes in territorial behavior in this species. We also examined the possibility that the probability or rate of attack on alien hyenas encountered within the clan's territory would vary with the sex of the intruders. Initiation and leadership of most cooperative territorial behaviors were by adult female clan members, although border patrols were occasionally conducted by groups composed exclusively of resident males. The vast majority of alien intruders into the territory of the study clan were males. Resident females were more likely to attack intruding females than intruding males, but hourly rates of aggression directed by females towards aliens did not vary with intruder sex. Resident males were more likely than resident females to attack alien males, and resident males directed significantly higher hourly rates of aggression towards intruding males than females. Although female leadership in most cooperative territorial behaviors distinguishes spotted hyenas from many mammalian carnivores, other sex differences in the territorial behavior of spotted hyenas resemble those documented in other gregarious predators. Sex differences observed in hyena territoriality are consistent with the hypothesis that male and female clan members derive different selective benefits from advertisement and defense of group territories.     

Endocrine correlates of pregnancy in the ring-tailed lemur (Lemur catta): implications for the masculinization of daughters

Female ring-tailed lemurs (Lemur catta) are Malagasy primates that are size monomorphic with males, socially dominate males, and exhibit a long, pendulous clitoris, channeled by the urethra. These masculine traits evoke certain attributes of female spotted hyenas (Crocuta crocuta) and draw attention to the potential role of androgens in lemur sexual differentiation. Here, hormonal correlates of prenatal development were assessed to explore the possibility that maternal androgens may shape the masculine morphological and behavioral features of developing female lemurs. Maternal serum 17α-hydroxyprogesterone, dehydroepiandrosterone sulphate (DHEA-S), ?⁴ androstenedione (androst-4-ene-3,17,dione), testosterone, and 17β-estradiol were charted throughout the 19 pregnancies of 11 ring-tailed lemurs. As in spotted hyenas, lemur pregnancies were associated with an immediate increase in androgen concentrations (implicating early maternal derivation), followed by continued increases across stages of gestation. Pregnancies that produced singleton males, twin males, or mixed-sex twins were marked by greater androgen and estrogen concentrations than were pregnancies that produced singleton or twin females, especially in the third trimester, implicating the fetal testes in late-term steroid profiles. Concentrations of DHEA-S were mostly below detectable limits, suggesting a minor role for the adrenals in androgen biosynthesis. Androgen concentrations of pregnant lemurs bearing female fetuses, although less than those of pregnant hyenas, exceeded preconception and postpartum values and peaked in the third trimester. Although a maternal (and, on occasion, fraternal) source of androgen may exist for fetal lemurs, further research is required to confirm that these steroids would reach the developing female and contribute to her masculinization.     

Defense of females, but not social status, predicts plasma androgen levels in male spotted hyenas

A positive correlation between male social status and testosterone levels is expected and often found in social species with high rates of agonistic interactions or when social relationships among males are unstable. In contrast, in species with low rates of agonistic interactions or when social relationships are stable, testosterone levels should not correlate with social status. The "challenge hypothesis" predicts that androgen levels should rise during periods of courtship or mate guarding. We addressed these questions in free-ranging spotted hyenas, a species with low rates and low intensities of aggression among males but where males spend extensive effort to court females. In males, we measured testosterone, its precursor androstenedione, and its metabolite 5alpha-dihydrotestosterone. As predicted, testosterone levels were significantly higher and androstenedione levels tended to be higher in males that, at the time of sampling, defended a female, compared with males that did not defend a female. Also, as predicted, there was no correlation between social status and androgen levels in male spotted hyenas.     

Androgens and the role of female "hyperaggressiveness" in spotted hyenas (Crocuta crocuta)

It has been suggested that female dominance in spotted hyenas evolved due to selection for "hyperaggressive" androgenized females. According to this view, virilized external genitalia of female hyenas developed as a byproduct of selection for "androgen-facilitated social dominance." The evidence that female hyenas have higher androgen levels than males or other female mammals is inconclusive. We compared concentrations of testosterone (T), 5alpha-dihydrotestosterone (DHT), and androstenedione (AE) from a population in the Serengeti. Females had significantly lower T and DHT levels than predispersal and postdispersal males. AE levels did not significantly differ between females and postdispersal males, but were significantly lower in predispersal males. Our results, and those from studies that have demonstrated that male and female hyenas experience similar levels of maternal androgens during fetal development, provide little support for a theory of selection for female dominance and hyperaggressiveness through enhanced secretion of androgens. Our data are consistent with an alternative view that female virilization is a byproduct of selection for precocial aggressive cubs of both sexes. According to this view, high investment in lactation favored selection for accelerated fetal development, high neonatal aggression, and facultative siblicide.     

Sexual mimicry in hyenas

Genital masculinization in female spotted hyenas has been widely explained as an incidental consequence of high androgen levels. High androgen levels, in turn, were supposed to be favored because they led to adaptive aggressive behavior. Incidental androgenization is no longer a tenable hypothesis, however, because genital masculinization has been shown to proceed in the absence of androgenic steroids. Thus, an alternative hypothesis is required. The genitals of spotted hyena females are not simply masculinized, but exhibit a detailed physical resemblance to the male genitalia. In the absence of satisfactory alternative explanations, we propose that selection may have favored sexual mimicry in females because they are more likely than males to be targets of aggression from other females. Male-like camouflage could theoretically be protective in three contexts: neonate sibling aggression, infanticide by conspecific females, and interclan territoriality. Current data suggest that if sexual mimicry is important, its effects are strongest among infants.     

Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure

Men and women differ on performance and strategy on several spatial tasks. Rodents display similar sex differences, and manipulations of early hormone exposure alter the direction of these differences. However, most cognitive testing of nonhuman primates has utilized sample sizes too small to investigate sexually differentiated behaviors. This study presents an investigation of sex differences and the effects of prenatal androgen on spatial memory and strategy use in rhesus monkeys. Monkeys prenatally exposed to vehicle, testosterone, or the androgen receptor blocker flutamide performed a search task in which 5 of 12 goal boxes contained food rewards. Spatial consistency and the presence of local landmarks were varied. Performance when both spatial and marker cues were available did not differ by sex or prenatal treatment. Contrary to predictions, females easily solved the task when local markers were removed, and their performance outscored males. Although eliminating spatial consistency and requiring subjects to use local markers impaired performance by all monkeys, females continued to locate correct goal boxes at higher than chance levels and scored better than males. Blocking prenatal androgen exposure in males improved use of local markers. These findings suggest that the tendency to attend to landmarks and to use them in solving spatial problems is typical of females across many species, including rodents, humans, and rhesus monkeys. In rhesus monkeys and rodents, developmental androgen eliminates this specialization. However, these results are the only known example of better performance of females than males when salient markers are removed.     

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Sexual differentiation in three unconventional mammals: spotted hyenas, elephants and tammar wallabies

The present review explores sexual differentiation in three non-conventional species: the spotted hyena, the elephant and the tammar wallaby, selected because of the natural challenges they present for contemporary understanding of sexual differentiation. According to the prevailing view of mammalian sexual differentiation, originally proposed by Alfred Jost, secretion of androgen and anti-Mullerian hormone (AMH) by the fetal testes during critical stages of development accounts for the full range of sexually dimorphic urogenital traits observed at birth. Jost's concept was subsequently expanded to encompass sexual differentiation of the brain and behavior. Although the central focus of this review involves urogenital development, we assume that the novel mechanisms described in this article have potentially significant implications for sexual differentiation of brain and behavior, a transposition with precedent in the history of this field. Contrary to the "specific" requirements of Jost's formulation, female spotted hyenas and elephants initially develop male-type external genitalia prior to gonadal differentiation. In addition, the administration of anti-androgens to pregnant female spotted hyenas does not prevent the formation of a scrotum, pseudoscrotum, penis or penile clitoris in the offspring of treated females, although it is not yet clear whether the creation of masculine genitalia involves other steroids or whether there is a genetic mechanism bypassing a hormonal mediator. Wallabies, where sexual differentiation occurs in the pouch after birth, provide the most conclusive evidence for direct genetic control of sexual dimorphism, with the scrotum developing only in males and the pouch and mammary glands only in females, before differentiation of the gonads. The development of the pouch and mammary gland in females and the scrotum in males is controlled by genes on the X chromosome. In keeping with the "expanded" version of Jost's formulation, secretion of androgens by the fetal testes provides the best current account of a broad array of sex differences in reproductive morphology and endocrinology of the spotted hyena, and androgens are essential for development of the prostate and penis of the wallaby. But the essential circulating androgen in the male wallaby is 5alpha androstanediol, locally converted in target tissues to DHT, while in the pregnant female hyena, androstenedione, secreted by the maternal ovary, is converted by the placenta to testosterone (and estradiol) and transferred to the developing fetus. Testicular testosterone certainly seems to be responsible for the behavioral phenomenon of musth in male elephants. Both spotted hyenas and elephants display matrilineal social organization, and, in both species, female genital morphology requires feminine cooperation for successful copulation. We conclude that not all aspects of sexual differentiation have been delegated to testicular hormones in these mammals. In addition, we suggest that research on urogenital development in these non-traditional species directs attention to processes that may well be operating during the sexual differentiation of morphology and behavior in more common laboratory mammals, albeit in less dramatic fashion.     

Sex Differences in Infant Rhesus Macaque Separation–Rejection Vocalizations and Effects of Prenatal Androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation–rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Post-weaning maternal effects and the evolution of female dominance in the spotted hyena

Mammalian societies in which females dominate males are rare, and the factors favouring the evolution of female dominance have yet to be clearly identified. We propose a new hypothesis for the evolution of female dominance and test its predictions with empirical data from the spotted hyena (Crocuta crocuta), a well-studied species characterized by female dominance. We suggest that constraints imposed by the development of a feeding apparatus specialized for bone cracking, in combination with the intensive feeding competition characteristic of spotted hyenas, led to the evolution of female dominance. Specifically, we propose that protracted development of the feeding apparatus in young hyenas led to selection for increased aggressiveness in females as a compensatory mechanism for mothers to secure food access for their young after weaning. Our analyses yielded results consistent with this hypothesis. Morphological and behavioural measurements indicate that skull development is indeed protracted in this species; spotted hyenas do not achieve adult skull size or feeding performance capabilities until after sexual maturity. The period between weaning and completed skull development is particularly challenging, as indicated by high mortality. Finally, maternal presence between weaning and full skull maturity, as well as the relative ability of females to aggressively displace conspecifics from food, are important determinants of offspring survival.     

Timing of prenatal androgen exposure: anatomical and endocrine effects on juvenile male and female rhesus monkeys

Prenatal androgen shapes genital differentiation. In humans, genital anatomy determines sex of rearing and subsequent behavioral development. Rhesus monkey genital anatomy and neuroendocrine function are sexually differentiated, and behavioral development occurs in a complex social environment. We investigated prenatal hormonal influences on sexual differentiation by suppressing or increasing androgens in male and female rhesus monkeys. Pregnant multiparous female rhesus monkeys received 35-40 days of testosterone enanthate (TE) treatment, androgen antagonist (flutamide, FL) treatment, or vehicle starting on gestation day (GD) 35 or 40 (early) or GD 110 or 115 (late). Exogenous androgen increased neonatal LH secretion in females when given early and altered female genital differentiation when administered either early or late. TE treatment, early or late in gestation, had no measurable effects on male genital differentiation or neuroendocrine function. Early FL treatment, however, radically altered male genital differentiation, producing in two cases males with a urethral opening separate from the glans. In females, early FL treatment produced detectable alterations in genitalia consistent with a reduced exposure to prenatal androgen, suggesting that female rhesus monkeys are naturally exposed prenatally to meaningful levels of T. Late FL treatment reduced male penis size and increased neonatal T secretion, but had no effect in females. This is the first study to block endogenous prenatal testosterone in rhesus monkeys, thereby altering sexual differentiation. These findings illustrate the complexity of prenatal influences on anatomical and neuroendocrine development. The relationship between the anatomical changes reported here and sex differences in behavior is currently under investigation.     

Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia

The ratio of the length of the second digit (2D) to the length of the fourth digit (4D) is greater in women than in men. Since androgens are involved in most somatic sex differences and since the sexual dimorphism in 2D:4D is stable from 2 years of age in humans, it was hypothesized that finger length pattern development might be affected by early androgen exposure. Human females with congenital adrenal hyperplasia (CAH) are exposed prenatally to higher than normal levels of adrenal androgens, providing an opportunity to test the effects of early androgen exposure on digit ratios. The 2D:4D was calculated for females with CAH, females without CAH, males with CAH, and males without CAH. Females with CAH had a significantly smaller 2D:4D on the right hand than did females without CAH. Males with CAH had a significantly smaller 2D:4D on the left hand than did males without CAH. A subset of six males with CAH had a significantly smaller 2D:4D on both hands compared with their male relatives without CAH. These results are consistent with the idea that prenatal androgen exposure reduces the 2D:4D and plays a role in the establishment of the sex difference in human finger length patterns. Finger lengths may therefore offer a retrospective marker of perinatal androgen exposure in humans.     

Sex differences in the play behavior of immature spotted hyenas, Crocuta crocuta

Social, locomotor, and object play were studied in a colony of five male and five female peer-reared spotted hyenas during 12 1-hr tests while the animals were 13-19 months of age. Animals were tested in both same-sex and mixed-sex groups and were stimulated to play by the introduction of fresh straw and sawdust bedding. Each test was videotaped and the frequency of each type of play was determined by a time sampling procedure. Females played more frequently than males, however, the category of play which was elevated depended upon the social context during testing. In same-sex tests the frequency of vigorous social play displayed by females markedly exceeded that by males, but no comparable sex difference appeared in mixed-sex tests. Females engaged in locomotor play more frequently than males in mixed-sex tests, but no comparable sex difference appeared in same-sex tests. No sex difference in object play was observed. Two male and two female hyenas were gonadectomized prior to the initiation of the present sequence of tests. The results suggest that gonadectomy during the prepubertal period does not affect the frequency of play behavior. However, the small sample sizes preclude any conclusive determination of the effects of these gonadectomies on play.     

Social and hormonal influences on behavior of adult male, female, and pseudohermaphroditic rhesus monkeys

We previously demonstrated that in a simple pair test situation the expression of adult male sexual behavior by rhesus monkeys depends on both prenatal (organizational) and adult (activational) androgen exposure. In the present study we used a more complex social situation (trio tests) to evaluate the behavior of males, females, and female pseudohermaphrodites. In these trio tests, the experimental subjects were tested with two estrogenized stimulus females simultaneously. Sex differences in behavior were made apparent by this complex testing situation that could not have emerged in the pair test. Gonadectomized males and female pseudohermaphrodites, but not ovariectomized females that were concurrently receiving TP, exhibited increased male sexual behavior in trio tests compared to pair tests. In trio tests, the males and pseudohermaphrodites showed evidence of partner preference by interacting almost exclusively with one of the two stimulus females. These "preferred females" in turn were responsible for the majority of the proceptive behavior exhibited in these tests. Ovariectomized females rarely displayed male sexual behavior in either test situation. These results further support the hypothesis that prenatal androgen exposure predisposes monkeys to exhibit masculine behavior traits when they reach adulthood and are exposed to the activational influences of androgens.     

Plasma androgens in spotted hyaenas (Crocuta crocuta): influence of social and reproductive development

Differences in plasma testosterone and androstenedione concentrations in male spotted hyaenas belonging to various reproductive and social categories 4 clans resident in South Africa and Botswana suggest that central-immigrant males have the highest concentrations of androgens, reflecting their roles as mating males. Social inhibition of reproductive function may occur in other males. A reversal in the ratio of testosterone: androstenedione occurs at puberty in most individuals, testosterone becoming the dominant hormone, especially in males that have procured mating rites. Cubs of either sex had low testosterone concentrations, except for a 4-day-old male that displayed adult concentrations, which were accompanied by a temporary testicular descent. Plasma testosterone concentrations in females largely reflected ovarian activity and showed no correlation with androstenedione concentrations. Female cubs had androstenedione concentrations significantly higher than those in all other social categories except for the central-immigrant males. The androgen profiles presented here suggest that the key to the behavioural dominance of female spotted hyaenas over males may lie with the neonatal developmental stages, rather than with the androgen patterns of adult animals.