Group size and mating system predict sex differences in vocal fundamental frequency in anthropoid primates.

Vocalizations differ substantially between the sexes in many primates, and low-frequency male vocalizations may be favored by sexual selection because they intimidate rivals and/or attract mates. Sexual dimorphism in fundamental frequency may be more pronounced in species with more intense male mating competition and in those with large group size, where social knowledge is limited and efficient judgment of potential mates and competitors is crucial. These non-mutually exclusive explanations have not been tested simultaneously across primate species. In a sample of vocalizations (n = 1914 recordings) across 37 anthropoid species, we investigated whether fundamental frequency dimorphism evolved in association with increased intensity of mating competition (H1), large group size (H2), multilevel social organization (H3), a trade-off against the intensity of sperm competition (H4), and/or poor acoustic habitats (H5), controlling for phylogeny and body size dimorphism. We show that fundamental frequency dimorphism increased in evolutionary transitions towards larger group size and polygyny. Findings suggest that low-frequency male vocalizations in primates may have been driven by selection to win mating opportunities by avoiding costly fights and may be more important in larger groups, where limited social knowledge affords advantages to rapid assessment of status and threat potential via conspicuous secondary sexual characteristics.

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.

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.

Evidence for Perinatal Steroid Influence on Human Sexual Orientation and Gendered Behavior.

In laboratory animals, exposure to gonadal steroid hormones before and immediately after birth can exert permanent effects on many behaviors, particularly reproductive behaviors. The extent to which such effects occur in humans remains an open question, but several lines of evidence indicate that perinatal levels of both androgens and estrogens may affect adult human psychology and behavior, including sexual orientation and gender nonconformity. Some putative indicators of prenatal androgen exposure, including the ratio of the length of the index finger to that of the ring finger (2D:4D), have repeatedly indicated that lesbians, on average, were exposed to more prenatal androgens than straight women, suggesting that sufficient fetal androgen exposure predisposes a fetus to gynephilia (attraction to women) at maturity. The digit ratios of gay men do not differ from those of straight men, suggesting that prenatal androgen levels are not responsible for their androphilia (attraction to men). However, evidence that gay men who prefer an insertive anal sex role (ASR) have more masculine digit ratios than those preferring a receptive ASR suggests that early androgens influence some sexual preferences in men. Furthermore, digit ratios among gay men have been found to correlate with recalled childhood gender nonconformity (CGN). People with isolated gonadotropin-releasing hormone (GnRH) deficiency (IGD) offer further insight into the effects of perinatal gonadal steroid exposure. In people with IGD, gonadal hormone production is low or absent after the first trimester of gestation. However, because placental gonadotropins drive gonadal hormone secretion during the first trimester when genitalia sexually differentiate, individuals with IGD are unambiguously male or female at birth, consistent with their chromosomal and gonadal sex. Men with IGD report greater CGN, again suggesting that perinatal androgen exposure contributes to male-typical behavioral patterns in humans. Interestingly, women with IGD report less androphilia and more bisexuality than control women, suggesting that perinatal ovarian steroids in females typically augment androphilia in adulthood. Taken together, these findings indicate that the perinatal hormonal milieu influences human sexual orientation and gender conformity.

Vocal modulation in human mating and competition.

The human voice is dynamic, and people modulate their voices across different social interactions. This article presents a review of the literature examining natural vocal modulation in social contexts relevant to human mating and intrasexual competition. Altering acoustic parameters during speech, particularly pitch, in response to mating and competitive contexts can influence social perception and indicate certain qualities of the speaker. For instance, a lowered voice pitch is often used to exert dominance, display status and compete with rivals. Changes in voice can also serve as a salient medium for signalling a person's attraction to another, and there is evidence to support the notion that attraction and/or romantic interest can be distinguished through vocal tones alone. Individuals can purposely change their vocal behaviour in attempt to sound more attractive and to facilitate courtship success. Several findings also point to the effectiveness of vocal change as a mechanism for communicating relationship status. As future studies continue to explore vocal modulation in the arena of human mating, we will gain a better understanding of how and why vocal modulation varies across social contexts and its impact on receiver psychology. This article is part of the theme issue 'Voice modulation: from origin and mechanism to social impact (Part I)'.

Evidence that perinatal ovarian hormones promote women's sexual attraction to men.

Ovarian estrogens may influence the development of the human brain and behavior, but there are few opportunities to test this possibility. Isolated GnRH deficiency (IGD) is a rare endocrine disorder that could provide evidence for the role of estrogens in organizing sexually differentiated phenotypes: Unlike typical development, development in individuals with IGD is characterized by low or absent gonadal hormone production after the first trimester of gestation. Because external genitalia develop in the first trimester, external appearance is nevertheless concordant with gonadal sex in people with IGD. We therefore investigated the effects of gonadal hormones on sexual orientation by comparing participants with IGD (n = 97) to controls (n = 1670). Women with IGD reported lower male-attraction compared with typically developing women. In contrast, no consistent sexuality differences between IGD and typically developing men were evident. Ovarian hormones after the first trimester appear to influence female-typical dimensions of sexual orientation.

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.

Linking human male vocal parameters to perceptions, body morphology, strength and hormonal profiles in contexts of sexual selection.

Sexual selection appears to have shaped the acoustic signals of diverse species, including humans. Deep, resonant vocalizations in particular may function in attracting mates and/or intimidating same-sex competitors. Evidence for these adaptive functions in human males derives predominantly from perception studies in which vocal acoustic parameters were manipulated using specialist software. This approach affords tight experimental control but provides little ecological validity, especially when the target acoustic parameters vary naturally with other parameters. Furthermore, such experimental studies provide no information about what acoustic variables indicate about the speaker-that is, why attention to vocal cues may be favored in intrasexual and intersexual contexts. Using voice recordings with high ecological validity from 160 male speakers and biomarkers of condition, including baseline cortisol and testosterone levels, body morphology and strength, we tested a series of pre-registered hypotheses relating to both perceptions and underlying condition of the speaker. We found negative curvilinear and negative linear relationships between male fundamental frequency (fo) and female perceptions of attractiveness and male perceptions of dominance. In addition, cortisol and testosterone negatively interacted in predicting fo, and strength and measures of body size negatively predicted formant frequencies (Pf). Meta-analyses of the present results and those from two previous samples confirmed that fonegatively predicted testosterone only among men with lower cortisol levels. This research offers empirical evidence of possible evolutionary functions for attention to men's vocal characteristics in contexts of sexual selection.

Pubertal timing predicts adult psychosexuality: Evidence from typically developing adults and adults with isolated GnRH deficiency.

Evidence suggests that psychosexuality in humans is modulated by both organizational effects of prenatal and peripubertal sex steroid hormones, and by activational effects of circulating hormones in adulthood. Experimental work in male rodents indicates that sensitivity to androgen-driven organization of sexual motivation decreases across the pubertal window, such that earlier puberty leads to greater sex-typicality. We test this hypothesis in typically developing men (n = 231) and women (n = 648), and in men (n = 72) and women (n = 32) with isolated GnRH deficiency (IGD), in whom the precise timing of peripubertal hormone exposure can be ascertained via the age at which hormone replacement therapy (HRT) was initiated. Psychosexuality was measured with the Sexual Desire Inventory-2 (SDI-2) and Sociosexual Orientation Inventory-Revised (SOI-R). In both sexes, earlier recalled absolute pubertal timing predicted higher psychosexuality in adulthood, although the magnitude of these associations varied with psychosexuality type and group (i.e., typically developing and IGD). Results were robust when controlling for circulating steroid hormones in typically developing participants. Age of initiation of HRT in men with IGD negatively predicted SOI-R. We discuss the clinical implications of our findings for conditions in which pubertal timing is medically altered.

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.

Operational Sex Ratio Predicts Binge Drinking Across U.S. Counties.

Previous research suggests that binge drinking among young men serves as a "costly signal" to potential mates, such that the binge drinker is capable of bearing the harmful consequences of alcohol consumption. Here, we propose that binge drinking among young adults is conditionally dependent upon the signaler's willingness to take risks, which is influenced by the local operational sex ratio (OSR). Using archived binge drinking estimates from 2009 to 2012 and Census Bureau records of OSRs, we tested the relationship between OSR and binge drinking rates at the county level across 3,143 U.S. counties against hypotheses drawn from evolutionary theory. Results from our mixed-effects models revealed that a higher overall OSR (i.e., more eligible men compared to women) was associated with higher male binge drinking rates but lower female binge drinking rates. A higher OSR particularly in the 20-29 and 50+ age groups predicted higher male binge drinking rates but lower female binge drinking rates. Our findings generally support predictions derived from evolutionary theory and suggest that binge drinking may function as a costly sexual signal, conditionally regulated by age and the local sex ratio.

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.

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.

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.

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.

Hadza Men With Lower Voice Pitch Have a Better Hunting Reputation.

Previous research with hunter-gatherers has found that women perceive men with voices manipulated to be lower in pitch to be better hunters, and men perceive women with lower pitch to be better gatherers. Here, we test if actual voice pitch is associated with hunting and gathering reputations in men and women, respectively. We find that voice pitch does relate to foraging reputation in men, but not in women, with better hunters having a lower voice pitch. In addition, we find that the previously documented relationship between voice pitch and reproductive success no longer holds when controlling for hunting reputation, but hunting reputation remains a significant predictor of reproductive success when controlling for voice pitch. This raises the possibility that voice pitch is being selected for in hunter-gatherers because of the relationship between voice pitch and hunting reputation.