Low Perinatal Androgens Predict Recalled Childhood Gender Nonconformity in Men.

The contributions of gonadal hormones to the development of human behavioral sex differences are subjects of intense scientific and social interest. Isolated gonadotropin-releasing-hormone deficiency (IGD) is a rare endocrine disorder that can reveal a possible role of early gonadal hormones. IGD is characterized by low or absent gonadal hormone production after the first trimester of gestation, but external genitalia and hence gender of rearing are concordant with chromosomal and gonadal sex. We investigated recalled childhood gender nonconformity in men (n = 65) and women (n = 32) with IGD and typically developing men (n = 463) and women (n = 1,207). Men with IGD showed elevated childhood gender nonconformity, particularly if they also reported undescended testes at birth, a marker of low perinatal androgens. Women with IGD did not differ from typically developing women. These results indicate that early androgen exposure after the first trimester contributes to male-typical gender-role behaviors in childhood.

Facial masculinity does not appear to be a condition-dependent male ornament and does not reflect MHC heterozygosity in humans.

Recent studies have called into question the idea that facial masculinity is a condition-dependent male ornament that indicates immunocompetence in humans. We add to this growing body of research by calculating an objective measure of facial masculinity/femininity using 3D images in a large sample (n = 1,233) of people of European ancestry. We show that facial masculinity is positively correlated with adult height in both males and females. However, facial masculinity scales with growth similarly in males and females, suggesting that facial masculinity is not exclusively a male ornament, as male ornaments are typically more sensitive to growth in males compared with females. Additionally, we measured immunocompetence via heterozygosity at the major histocompatibility complex (MHC), a widely-used genetic marker of immunity. We show that, while height is positively correlated with MHC heterozygosity, facial masculinity is not. Thus, facial masculinity does not reflect immunocompetence measured by MHC heterozygosity in humans. Overall, we find no support for the idea that facial masculinity is a condition-dependent male ornament that has evolved to indicate immunocompetence.

Relationships between ovarian hormone concentrations and mental rotations performance in naturally-cycling women.

Circulating gonadal hormones have been linked to variation in the structure and function of the adult human brain, raising the question of how cognition is affected by sex hormones in adulthood. The impacts of progestogens and estrogens are of special interest due to the widespread use of hormone supplementation. Multiple studies have analyzed relationships between ovarian hormones and mental rotation performance, one of the largest known cognitive sex differences; however, results are conflicting. These discrepancies are likely due in part to modest sample sizes and reliance on self-report measures to assess menstrual cycle phase. The present study aimed to clarify the impact of progestogens and estrogens on visuospatial cognition by relating mental rotation task performance to salivary hormone concentrations. Across two studies totaling 528 naturally-cycling premenopausal women, an internal meta-analysis suggested a small, positive effect of within-subjects changes in progesterone on MRT performance (estimate = 0.44, p = 0.014), though this result should be interpreted with caution given multiple statistical analyses. Between-subjects differences and within-subject changes in estradiol did not significantly predict MRT. These results shed light on the potential cognitive effects of endogenous and exogenous hormone action, and the proximate mechanisms modulating spatial cognition.

No evidence that hormonal contraceptive use or circulating sex steroids predict complex emotion recognition.

Relatively little is known about the effects of endogenous and exogenous steroid hormones on ecologically relevant behavioral and cognitive phenotypes in women, such as emotion recognition, despite the widespread use of steroid hormone-altering hormonal contraceptives (HCs). Though some previous studies have examined the effect of HC use, estradiol, progesterone, and testosterone on emotion recognition in women, they have been limited by cross-sectional designs, small sample sizes (total n < 100), and compromised statistical power to detect significant effects. Using data from two test sessions in a large sample of naturally cycling women (NC; n = 192) and women on HCs (n = 203), we found no group differences in emotion recognition; further, the lack of group differences in emotion recognition was not modulated by item difficulty or emotional valence. Among NC women who provided saliva samples across two sessions that were assayed for estradiol and progesterone concentrations, we found no compelling evidence across models that between-subject differences and within-subject fluctuations in these ovarian hormones predicted emotion recognition accuracy, with the exception that between-subjects estradiol negatively predicted emotion recognition for emotions of neutral valence (p = .042). Among HC women who provided saliva samples across two sessions that were assayed for testosterone, we found no compelling evidence that between-subjects differences and within-subject fluctuations in testosterone predicted emotion recognition accuracy. Overall, our analyses provide little support for the idea that circulating endogenous or exogenous ovarian hormones influence emotion recognition in women.

Visual cues to fertility are in the eye (movements) of the beholder.

Past work demonstrates that humans behave differently towards women across their menstrual cycles, even after exclusively visual exposure to women's faces. People may look at women's faces differently as a function of women's menstrual cycles. Analyses of participants' scanpaths (eye movement patterns) while they looked at women at different phases of their menstrual cycles revealed that observers exhibit more consistent scanpaths when examining women's faces when women are in a menstrual cycle phase that typically corresponds with peak fertility, whereas they exhibit more variable patterns when looking at women's faces when they are in phases that do not correspond with fertility. A multivariate classifier on participants' scanpaths predicted whether they were looking at the face of a woman in a more typically fertile- versus non-fertile-phase of her menstrual cycle with above-chance accuracy. These findings demonstrate that people look at women's faces differently as a function of women's menstrual cycles, and suggest that people are sensitive to fluctuating visual cues associated with women's menstrual cycle phase.

Menstrual cycle phase predicts women's hormonal responses to sexual stimuli.

A robust body of research has demonstrated shifts in women's sexual desire and arousal across the menstrual cycle, with heightened desire and arousal coincident with heightened probability of conception (POC), and it is likely that ovarian hormones modulate these shifts. However, studies in which women are exposed to audiovisual sexual stimuli (AVSS) at high POC (mid-follicular) and low POC (luteal) phases have failed to detect significant differences in genital or subjective arousal patterns based on menstrual cycle phase. Here, we tested whether hormonal responsivity to AVSS differs as a function of cycle phase at testing, and whether phase during which participants were first exposed to AVSS influences hormonal responsivity in subsequent test sessions. Twenty-two naturally cycling heterosexual women were exposed to AVSS during the follicular and luteal phases, with phase at first test session counterbalanced across participants. Salivary samples were collected before and after AVSS exposure. Estradiol increased significantly during both follicular and luteal phase sessions, and increases were higher during the follicular phase. Testosterone (T) increased significantly only during the follicular phase session, while progesterone (P) did not change significantly during either cycle phase. Session order and current cycle phase interacted to predict P and T responses, such that P and T increased during the follicular phase in women who were first tested during the luteal phase. These data suggest that menstrual cycle phase influences hormonal responsivity to AVSS, and contribute to a growing body of clinical and empirical literature on the neuroendocrine modulators of women's sexuality.

Do women's preferences for masculine voices shift across the ovulatory cycle?

Are estrous mate preference shifts robust? This question is the subject of controversy within human evolutionary sciences. For nearly two decades, mate preference shifts across the ovulatory cycle were considered an important feature of human sexual selection, directing women's attention toward mates with indicators of "good genes" in their fertile phase, when conception is possible. However, several recent studies on masculine faces, bodies and behaviors did not find evidence supporting this account, known as the good genes ovulatory shift hypothesis. Furthermore, evidence that preferences for masculine characteristics in men's voices are related to women's cycle phase and hormonal status is still equivocal. Here, we report two independent within-subject studies from different labs with large sample sizes (N = 202 tested twice in Study 1; N = 157 tested four times in Study 2) investigating cycle shifts in women's preferences for masculine voices. In both studies, hormonal status was assessed directly using salivary assays of steroid hormones. We did not find evidence for effects of cycle phase, conception risk, or steroid hormone levels on women's preferences for masculine voices. Rather, our studies partially provide evidence for cycle shifts in women's general attraction to men's voices regardless of masculine characteristics. Women's relationship status and self-reported stress did not moderate these findings, and the hormonal pattern that influences these shifts remains somewhat unclear. We consider how future work can clarify the mechanisms underlying psychological changes across the ovulatory cycle.

Are there vocal cues to human developmental stability? Relationships between facial fluctuating asymmetry and voice attractiveness.

Fluctuating asymmetry (FA), deviation from perfect bilateral symmetry, is thought to reflect an organism's relative inability to maintain stable morphological development in the face of environmental and genetic stressors. Previous research has documented negative relationships between FA and attractiveness judgments in humans, but scant research has explored relationships between the human voice and this putative marker of genetic quality in either sex. Only one study (and in women only) has explored relationships between vocal attractiveness and asymmetry of the face, a feature-rich trait space central in prior work on human genetic quality and mate choice. We therefore examined this relationship in three studies comprising 231 men and 240 women from two Western samples as well as Hadza hunter-gatherers of Tanzania. Voice recordings were collected and rated for attractiveness, and FA was computed from two-dimensional facial images as well as, for a subset of men, three-dimensional facial scans. Through meta-analysis of our results and those of prior studies, we found a negative association between FA and vocal attractiveness that was highly robust and statistically significant whether we included effect sizes from previously published work, or only those from the present research, and regardless of the inclusion of any individual sample or method of assessing FA (e.g., facial or limb FA). Weighted mean correlations between FA and vocal attractiveness across studies were -.23 for men and -.29 for women. This research thus offers strong support for the hypothesis that voices provide cues to genetic quality in humans.

Endocrinology of human female sexuality, mating, and reproductive behavior.

Hormones orchestrate and coordinate human female sexual development, sexuality, and reproduction in relation to three types of phenotypic changes: life history transitions such as puberty and childbirth, responses to contextual factors such as caloric intake and stress, and cyclical patterns such as the ovulatory cycle. Here, we review the endocrinology underlying women's reproductive phenotypes, including sexual orientation and gender identity, mate preferences, competition for mates, sex drive, and maternal behavior. We highlight distinctive aspects of women's sexuality such as the possession of sexual ornaments, relatively cryptic fertile windows, extended sexual behavior across the ovulatory cycle, and a period of midlife reproductive senescence-and we focus on how hormonal mechanisms were shaped by selection to produce adaptive outcomes. We conclude with suggestions for future research to elucidate how hormonal mechanisms subserve women's reproductive phenotypes.

Modeling 3D facial shape from DNA.

Human facial diversity is substantial, complex, and largely scientifically unexplained. We used spatially dense quasi-landmarks to measure face shape in population samples with mixed West African and European ancestry from three locations (United States, Brazil, and Cape Verde). Using bootstrapped response-based imputation modeling (BRIM), we uncover the relationships between facial variation and the effects of sex, genomic ancestry, and a subset of craniofacial candidate genes. The facial effects of these variables are summarized as response-based imputed predictor (RIP) variables, which are validated using self-reported sex, genomic ancestry, and observer-based facial ratings (femininity and proportional ancestry) and judgments (sex and population group). By jointly modeling sex, genomic ancestry, and genotype, the independent effects of particular alleles on facial features can be uncovered. Results on a set of 20 genes showing significant effects on facial features provide support for this approach as a novel means to identify genes affecting normal-range facial features and for approximating the appearance of a face from genetic markers.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids.

In many primates, including humans, the vocalizations of males and females differ dramatically, with male vocalizations and vocal anatomy often seeming to exaggerate apparent body size. These traits may be favoured by sexual selection because low-frequency male vocalizations intimidate rivals and/or attract females, but this hypothesis has not been systematically tested across primates, nor is it clear why competitors and potential mates should attend to vocalization frequencies. Here we show across anthropoids that sexual dimorphism in fundamental frequency (F0) increased during evolutionary transitions towards polygyny, and decreased during transitions towards monogamy. Surprisingly, humans exhibit greater F0 sexual dimorphism than any other ape. We also show that low-F0 vocalizations predict perceptions of men's dominance and attractiveness, and predict hormone profiles (low cortisol and high testosterone) related to immune function. These results suggest that low male F0 signals condition to competitors and mates, and evolved in male anthropoids in response to the intensity of mating competition.

Self-Reported Sexual Behavioral Interests and Polymorphisms in the Dopamine Receptor D4 (DRD4) Exon III VNTR in Heterosexual Young Adults.

Polymorphisms in the dopamine D4 receptor (DRD4) have previously been shown to associate with a variety of human behavioral phenotypes, including ADHD pathology, alcohol and tobacco craving, financial risk-taking in males, and broader personality traits such as novelty seeking. Recent research has linked the presence of a 7-repeat (7R) allele in a 48-bp variable number of tandem repeats (VNTR) along exon III of DRD4 to age at first sexual intercourse, sexual desire, arousal and function, and infidelity and promiscuity. We hypothesized that carriers of longer DRD4 alleles may report interest in a wider variety of sexual behaviors and experiences than noncarriers. Participants completed a 37-item questionnaire measuring sexual interests as well as Cloninger's Temperament and Character Inventory, and were genotyped for the 48-bp VNTR on exon III of DRD4. Based on our final genotyped sample of female (n = 139) and male (n = 115) participants, we found that 7R carriers reported interest in a wider variety of sexual behaviors (r = 0.16) within a young adult heterosexual sample of European descent. To our knowledge, this is the first reported association between DRD4 exon III VNTR genotype and interest in a variety of sexual behaviors. We discuss these findings within the context of DRD4 research and broader trends in human evolutionary history.

The face of female dominance: Women with dominant faces have lower cortisol.

The human face displays a wealth of information, including information about dominance and fecundity. Dominance and fecundity are also associated with lower concentrations of the stress hormone cortisol, suggesting that cortisol may negatively predict facial dominance and attractiveness. We digitally photographed 61 women's faces, had these images rated by men and women for dominance, attractiveness, and femininity, and explored relationships between these perceptions and women's salivary cortisol concentrations. In a first study, we found that women with more dominant-appearing, but not more attractive, faces had lower cortisol levels. These associations were not due to age, ethnicity, time since waking, testosterone, or its interaction with cortisol. In a second study, composite images of women with low cortisol were perceived as more dominant than those of women with high cortisol significantly more often than chance by two samples of viewers, with a similar but non-significant trend in a third sample. However, data on perceptions of attractiveness were mixed; low-cortisol images were viewed as more attractive by two samples of US viewers and as less attractive by a sample of Mexican viewers. Our results suggest that having a more dominant-appearing face may be associated with lower stress and hence lower cortisol in women, and provide further evidence regarding the information content of the human face.

Fulfilling desire: evidence for negative feedback between men's testosterone, sociosexual psychology, and sexual partner number.

Across human societies and many nonhuman animals, males have greater interest in uncommitted sex (more unrestricted sociosexuality) than do females. Testosterone shows positive associations with male-typical sociosexual behavior in nonhuman animals. Yet, it remains unclear whether the human sex difference in sociosexual psychology (attitudes and desires) is mediated by testosterone, whether any relationships between testosterone and sociosexuality differ between men and women, and what the nature of these possible relationships might be. In studies to resolve these questions, we examined relationships between salivary testosterone concentrations and sociosexual psychology and behavior in men and women. We measured testosterone in all men in our sample, but only in those women taking oral contraception (OC-using women) in order to reduce the influence of ovulatory cycle variation in ovarian hormone production. We found that OC-using women did not differ from normally-ovulating women in sociosexual psychology or behavior, but that circulating testosterone mediated the sex difference in human sociosexuality and predicted sociosexual psychology in men but not OC-using women. Moreover, when sociosexual psychology was controlled, men's sociosexual behavior (number of sexual partners) was negatively related to testosterone, suggesting that testosterone drives sociosexual psychology in men and is inhibited when those desires are fulfilled. This more complex relationship between androgens and male sexuality may reconcile some conflicting prior reports.

Does menstrual cycle phase influence the gender specificity of heterosexual women's genital and subjective sexual arousal?

Unlike men, heterosexual women's genital arousal is gender nonspecific, such that heterosexual women show relatively similar genital arousal to sexual stimuli depicting men and women but typically report greater subjective arousal to male stimuli. Based on the ovulatory-shift hypothesis-that women show a mid-cycle shift in preferences towards more masculine features during peak fertility-we predicted that heterosexual women's genital and subjective arousal would be gender specific (more arousal towards male stimuli) during peak fertility. Twenty-two naturally-cycling heterosexual women were assessed during the follicular and luteal phases of their menstrual cycle to examine the role of menstrual cycle phase in gender specificity of genital and subjective sexual arousal. Menstrual cycle phase was confirmed with salivary hormone assays; phase at the time of first testing was counterbalanced. Women's genital and subjective sexual arousal patterns were gender nonspecific, irrespective of cycle phase. Cycle phase at first testing session did not influence genital or subjective arousal in the second testing session. Similar to previous research, women's genital and subjective sexual arousal varied with cues of sexual activity, but neither genital nor subjective sexual arousal varied by gender cues, with the exception of masturbation stimuli, where women showed higher genital arousal to the stimuli depicting male compared to female actors. These data suggest that menstrual cycle phase does not influence the gender specificity of heterosexual women's genital and subjective sexual arousal.

Women's attractiveness changes with estradiol and progesterone across the ovulatory cycle.

In many species, females are more sexually attractive to males near ovulation. Some evidence suggests a similar pattern in humans, but methodological limitations prohibit firm conclusions at present, and information on physiological mechanisms underlying any such pattern is lacking. In 202 normally-cycling women, we explored whether women's attractiveness changed over the cycle as a function of two likely candidates for mediating these changes: estradiol and progesterone. We scheduled women to attend one session during the late follicular phase and another during the mid-luteal phase. At each session, facial photographs, voice recordings and saliva samples were collected. All photographs and voice recordings were subsequently rated by men for attractiveness and by women for flirtatiousness and attractiveness to men. Saliva samples were assayed for estradiol and progesterone. We found that progesterone and its interaction with estradiol negatively predicted vocal attractiveness and overall (facial plus vocal) attractiveness to men. Progesterone also negatively predicted women's facial attractiveness to men and female-rated facial attractiveness, facial flirtatiousness and vocal attractiveness, but not female-rated vocal flirtatiousness. These results strongly suggest a pattern of increased attractiveness during peak fertility in the menstrual cycle and implicate estradiol and progesterone in driving these changes.

Self-reported sexual desire in homosexual men and women predicts preferences for sexually dimorphic facial cues.

Recent studies investigating the relationship between self-reported sexual desire and attraction to same- and opposite-sex individuals have found that homosexual men's sexual desire is positively correlated with their self-reported attraction to own-sex individuals only, while homosexual women's sexual desire is positively correlated with their self-reported attraction to both men and women. These data have been interpreted as evidence that sexual desire strengthens men's pre-existing (i.e., dominant) sexual behaviors and strengthens women's sexual behaviors in general. Here we show that homosexual men's (n = 106) scores on the Sexual Desire Inventory-2 (SDI-2) were positively correlated with their preferences for exaggerated sex-typical shape cues in own-sex, but not opposite-sex, faces. Contrary to the hypothesis that sexual desire strengthens women's preferences for sexual dimorphism generally, homosexual women's (n = 83) SDI-2 scores were positively correlated with their preferences for exaggerated sex-typical shape cues in opposite-sex faces only. Together with previous research in heterosexual subjects, our findings support the proposal that sexual desire increases the incidence of existing sexual behaviors in homosexual and heterosexual men, and increases the incidence of sexual responses more generally in heterosexual women, although not necessarily in homosexual women.

Articulatory effects on perceptions of men's status and attractiveness.

Research on heterosexual mating has demonstrated that acoustic parameters (e.g., pitch) of men's voices influence their attractiveness to women and appearance of status and formidability to other men. However, little is known about how men's tendency to clearly articulate their speech influences these important social perceptions. In the current study, we used a repeated-measures design to investigate how men's articulatory clarity or conformity influenced women's (N = 45) evaluations of men's attractiveness for both short- and long-term relationships, and men's (N = 46) evaluations of physical formidability and prestige. Results largely supported our hypotheses: men who enunciated phonemes more distinctly were more attractive to women for long-term relationships than short-term relationships and were perceived by other men to have higher prestige than physical dominance. These findings suggest that aspects of articulatory behavior that influence perceptions of prestige and long-term mating attractiveness may indicate an early social history characterized by high socioeconomic status, likely owing to crystallization of articulatory patterns during the critical period of language development. These articulatory patterns may also be honest signals of condition or disposition owing to the nature of complex, multicomponent traits, which deserve further empirical attention.