David A. Puts

The Role of Androgen Receptors in the Masculinization of Brain and Behavior: What we’ve learned from the Testicular Feminization Mutation

Many studies demonstrate that exposure to testicular steroids such as testosterone early in life masculinizes the developing brain, leading to permanent changes in behavior. Traditionally, masculinization of the rodent brain is believed to depend on estrogen receptors (ERs) and not androgen receptors (ARs). According to the aromatization hypothesis, circulating testosterone from the testes is converted locally in the brain by aromatase to estrogens, which then activate ERs to masculinize the brain. However, an emerging body of evidence indicates that the aromatization hypothesis cannot fully account for sex differences in brain morphology and behavior, and that androgens acting on ARs also play a role. The testicular feminization mutation (Tfm) in rodents, which produces a nonfunctional AR protein, provides an excellent model to probe the role of ARs in the development of brain and behavior. Tfm rodent models indicate that ARs are normally involved in the masculinization of many sexually dimorphic brain regions and a variety of behaviors, including sexual behaviors, stress response and cognitive processing. We review the role of ARs in the development of the brain and behavior, with an emphasis on what has been learned from Tfm rodents as well as from related mutations in humans causing complete androgen insensitivity.

Masculine voices signal men's threat potential in forager and industrial societies

Humans and many non-human primates exhibit large sexual dimorphisms in vocalizations and vocal anatomy. In humans, same-sex competitors and potential mates attend to acoustic features of male vocalizations, but vocal masculinity especially increases perceptions of physical prowess. Yet, the information content of male vocalizations remains obscure. We therefore examined relationships between sexually dimorphic acoustic properties and mens threat potential. We first introduce a new measure of the structure of vocal formant frequencies, ‘formant position’ (Pf), which we show is more sexually dimorphic and more strongly related to height than is the most widely used measure of formant structure, ‘formant dispersion’, in both a US sample and a sample of Hadza foragers from Tanzania. We also show large sexual dimorphisms in the mean fundamental frequency (F0) and the within-utterance standard deviation in F0 (F0 − s.d.) in both samples. We then explore relationships between these acoustic parameters and mens body size, strength, testosterone and physical aggressiveness. Each acoustic parameter was related to at least one measure of male threat potential. The most dimorphic parameters, F0 and Pf, were most strongly related to body size in both samples. In the US sample, F0 predicted testosterone levels, Pf predicted upper body strength and F0 − s.d. predicted physical aggressiveness.

Cyclic variation in women’s preferences for masculine traits

Women’s preferences for several male traits, including voices, change over the menstrual cycle, but the proximate causes of these changes are unknown. This paper explores relationships between levels of estradiol, progesterone, luteinizing hormone, follicle stimulating hormone, prolactin, and testosterone (estimated using menstrual cycle information) and women’s preferences for male vocal masculinity in normally cycling and hormonally contracepting heterosexual females. Preferences for vocal masculinity decreased with predicted progesterone levels and increased with predicted prolactin levels in normally cycling—but not hormonally contracepting—women. Adaptive explanations for menstrual variation in women’s preferences for masculine traits are discussed and evaluated in light of these findings.

Sexual Orientation and the Second to Fourth Finger Length Ratio: A Meta-Analysis in Men and Women

The ratio of the lengths of the second and fourth fingers (2D:4D) may serve as a marker for prenatal androgen signaling. Because people are typically unaware of their 2D:4D, its use allows possible effects of early sex hormone regimes and socialization to be disentangled. We conducted a meta-analysis on relationships between 2D:4D and sexual orientation in men and women in 18 independent samples of men and 16 independent samples of women. Collectively, these samples comprised 1,618 heterosexual men, 1,693 heterosexual women, 1,503 gay men, and 1,014 lesbians. In addition to identifying the normative heterosexual sex difference in 2D:4D for both hands, we found that heterosexual women had higher (more feminine) left- and right-hand 2D:4D than did lesbians, but we found no difference between heterosexual and gay men. Moderator analyses suggested that ethnicity explained some between-studies variation in men. These results add to a literature suggesting that early sex hormone signaling affects sexual orientation in women, and highlight the need for further research exploring the relationships among 2D:4D, sexual orientation, and ethnicity in men.

Sexual Selection on Human Faces and Voices

Humans are highly sexually dimorphic primates, and some of the most conspicuous human sex differences occur in the face and voice. Consequently, this article utilizes research findings on human faces and voices to illustrate how human sex differences may have arisen by sexual selection (i.e., the type of natural selection favoring traits that increase mating opportunities). Evidence suggesting that sexual selection shaped womens faces and voices is reviewed. However, sexual selection likely operated more strongly on men over human evolution. Thus, this research focuses on two types of sexual selection operating on men: female mate choice, which favors traits that attract females, and male contests, which favor traits for excluding competitors from mates by force or threat of force. This article demonstrates how masculine faces and voices advertize critical information about mens mate value and threat potential, and reviews evidence that womens preferences and mens deference to masculine faces and voices reflect this information content. Data suggesting that facial and vocal masculinity influences mens mating opportunities and reproduction are discussed, and the article concludes by highlighting directions for future research.

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.

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 womens 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 womens 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.

Different Vocal Parameters Predict Perceptions of Dominance and Attractiveness

Low mean fundamental frequency (F0) in men’s voices has been found to positively influence perceptions of dominance by men and attractiveness by women using standardized speech. Using natural speech obtained during an ecologically valid social interaction, we examined relationships between multiple vocal parameters and dominance and attractiveness judgments. Male voices from an unscripted dating game were judged by men for physical and social dominance and by women in fertile and non-fertile menstrual cycle phases for desirability in short-term and long-term relationships. Five vocal parameters were analyzed: mean F0 (an acoustic correlate of vocal fold size), F0 variation, intensity (loudness), utterance duration, and formant dispersion (Df, an acoustic correlate of vocal tract length). Parallel but separate ratings of speech transcripts served as controls for content. Multiple regression analyses were used to examine the independent contributions of each of the predictors. Physical dominance was predicted by low F0 variation and physically dominant word content. Social dominance was predicted only by socially dominant word content. Ratings of attractiveness by women were predicted by low mean F0, low Df, high intensity, and attractive word content across cycle phase and mating context. Low Df was perceived as attractive by fertile-phase women only. We hypothesize that competitors and potential mates may attend more strongly to different components of men’s voices because of the different types of information these vocal parameters provide.

A sex difference in the predisposition for physical competition: males play sports much more than females even in the contemporary U.S.

Much evidence indicates that men experienced an evolutionary history of physical competition, both one-on-one and in coalitions. We thus hypothesized that, compared to girls and women, boys and men will possess a greater motivational predisposition to be interested in sports, especially team sports. According to most scholars, advocacy groups, and the United States courts, however, this hypothesis is challenged by modest sex differences in organized school sports participation in the contemporary U.S., where females comprise 42% of high school participants and 43% of intercollegiate participants. We conducted three studies to test whether organized school sports participation data underestimate the actual sex difference in sports participation. Study 1 analyzed the American Time Use Survey, which interviewed 112,000 individuals regarding their activities during one day. Females accounted for 51% of exercise (i.e., non-competitive) participations, 24% of total sports participations, and 20% of team sports participations. These sex differences were similar for older and younger age groups. Study 2 was based on systematic observations of sports and exercise at 41 public parks in four states. Females accounted for 37% of exercise participations, 19% of individual sports participations, and 10% of team sports participations. Study 3 involved surveying colleges and universities about intramural sports, which primarily consist of undergraduate participation in team sports. Across 34 institutions, females accounted for 26% of registrations. Nine institutions provided historical data, and these did not indicate that the sex difference is diminishing. Therefore, although efforts to ensure more equitable access to sports in the U.S. (i.e., Title IX) have produced many benefits, patterns of sports participation do not challenge the hypothesis of a large sex difference in interest and participation in physical competition.

Vocal masculinity is a robust dominance signal in men

Dominance assessment is important in mating competition across a variety of species, but little is known about how individuals’ own quality affects their assessment of potential rivals. We conducted two studies to test whether men’s own dominance affects their attentiveness to a putative dominance signal, vocal masculinity, when assessing competitors. Study I examined dominance ratings made by men in relation to their self-rated physical dominance. Study II examined dominance ratings made by men in relation to objective measures of their physical dominance, including size, strength, testosterone, and physical aggressiveness. Vocal masculinity strongly affected dominance ratings, but a man’s own dominance did not alter his attention to vocal masculinity when assessing dominance. However, men who rated themselves high on physical dominance rated the voices of other men lower on dominance and reported more sex partners (study I). Men with intermediate testosterone concentrations rated the voices of other men lower on dominance (study II). These results confirm the effect of vocal masculinity on dominance perceptions, provide further evidence that dominance is relevant to mating success, and shed new light on how men assess the dominance of rivals and potential allies. Our results suggest that attention to dominance signals may depend less on the observer’s own dominance in species with coalitional aggression, where individuals must assess others not only in relation to themselves but also in relation to each other. Among men, the effect of a deep, masculine voice on perceptions of dominance appears to be robust and unmediated by the formidability of the listener.