Testosterone is positively and estradiol negatively associated with mucosal immunity in Amazonian adolescents.

OBJECTIVES: A core assumption of life history theory and the immunocompetence handicap hypothesis (ICHH) is that testosterone (T) upregulates energetic investment in mating effort at the expense of immunity. This tenet, along with observed positive relationships between estrogens and immunity, may contribute to the higher observed morbidity and mortality of males. In the present study, we examine the association between sex steroid hormones and mucosal immunity as well as sex differences in immunity in a rural Amazonian population of immune-challenged Bolivian adolescents. METHODS: Salivary steroid hormones (T [males only] and estradiol [E2 , females only]), Tsimane-specific age-standardized BMI z-scores, and salivary mucosal immunity (sIgA, secretory IgA) were measured in 89 adolescent males and females. RESULTS: Males had significantly higher sIgA levels than females, which may be due to the observed immune-endocrine associations found in the present study. Controlling for age and phenotypic condition, higher T significantly predicted higher sIgA; whereas higher E2 was associated with lower sIgA in females. CONCLUSIONS: Results stood in contrast to common interpretations of the ICHH, that is, that T should be inversely associated with immunity. Findings from the present study support the notion that the endocrine system likely affects immunity in a regulatory fashion, upregulating certain aspects of immunity while downregulating others. An important remaining question is the adaptive reason(s) for sex differences in endocrine-mediated immuno-redistribution.

Adrenal maturation, nutritional status, and mucosal immunity in Bolivian youth.

OBJECTIVES: Humans-and several other apes-exhibit a unique pattern of post-natal adrenal maturation; however, the causes and consequences of variation in adrenal development are not well understood. In this study, we examine developmental and age-related maturation of the adrenal gland (measured via dehydroepiandrosterone-sulfate [DHEA-S]) for potential life-history associations with growth and mucosal immunity in a rural population of immune-challenged Bolivian juveniles and adolescents. METHODS: Salivary DHEA-S, anthropometrics, and salivary mucosal immunity (secretory IgA [sIgA]) were measured in 171 males and females, aged 8-23. RESULTS: Males with greater energy (i.e. fat) stores showed higher DHEA-S levels. Controlling for age and energetic condition (to control for phenotypic correlation), higher DHEA-S was associated with higher mucosal immunity (sIgA) among both males and females. Higher DHEA-S levels were positively associated with growth (i.e. height and strength) in males. CONCLUSIONS: In accordance with predictions derived from life-history theory, males with higher energy stores secrete more adrenal androgens. This suggests that adrenal maturation is costly and subject to constraints; that is, only males with sufficient reserves will invest in accelerated adrenal maturation. Further, DHEA-S appears to have a measureable influence on immunocompetence in adolescent males and females; therefore, deficits in DHEA-S may have important consequences for health and maturation during this period. Adrenal maturation is an important, but understudied component of human growth and development.

Maternal milk DHA content predicts cognitive performance in a sample of 28 nations.

Convergent evidence from neuronal biology and hominin brain hypertrophy suggests that omega-3 fatty acids are a limiting resource for neural and cognitive development in Homo sapiens, and therefore that children from populations with higher omega-3 availability should display superior cognitive performance. Using multiple regression, we tested this prediction in a sample of 28 countries, with Programme for International Student Assessment (PISA) math scores in 2009 as an index of cognitive performance, and country-specific breast milk levels of omega-3 docosahexaenoic acid (DHA) as an index of omega-3 availability. Breast milk DHA makes a highly significant contribution to math scores (ß = 0.462, P = 0.006), greater in magnitude than the control variables of per capita Gross Domestic Product (PCGDP) and educational expenditures per pupil. Together, dietary fish (positively) and total fat (negatively) explain 61% of the variance in maternal milk DHA in a larger sample of 39 countries.

Sex difference in travel is concentrated in adolescence and tracks reproductive interests.

Sexual selection theory suggests that the sex with a higher potential reproductive rate will compete more strongly for access to mates. Stronger intra-sexual competition for mates may explain why males travel more extensively than females in many terrestrial vertebrates. A male-bias in lifetime distance travelled is a purported human universal, although this claim is based primarily on anecdotes. Following sexual maturity, motivation to travel outside the natal territory may vary over the life course for both sexes. Here, we test whether travel behaviour among Tsimane forager-horticulturalists is associated with shifting reproductive priorities across the lifespan. Using structured interviews, we find that sex differences in travel peak during adolescence when men and women are most intensively searching for mates. Among married adults, we find that greater offspring dependency load is associated with reduced travel among women, but not men. Married men are more likely to travel alone than women, but only to the nearest market town and not to other Tsimane villages. We conclude that men's and women's travel behaviour reflects differential gains from mate search and parenting across the life course.

Functional variation in sensitivity to cues that a partner is cheating with a rival.

The costs imposed by a romantic partner's mixed reproductive strategy (MRS) generate selection pressures for anticipatory responses to mitigate or avoid those costs. People will differ in their vulnerability to those costs, based in part on the qualities of their romantic rivals. Thus, we predicted that individuals at high risk of a partner's MRS--women with many sexually accessible rivals and men with many rivals more physically attractive than themselves--would be more attentive to cues that an MRS was being employed than those at lower risk. Based on similarity judgments derived from a successive-pile-sort method, this prediction was supported in a study involving over 1,300 students and community members. These results complement a growing body of research on selection pressures generated by romantic rivals.

Voice change as a new measure of male pubertal timing: a study among Bolivian adolescents.

BACKGROUND: Age at menarche is often used to measure maturational tempo in girls. Unfortunately, no parallel marker exists for boys. It is suggested that voice change has a number of advantages as a marker of the timing and degree of male pubertal development. AIM: Traditional auxological methods are applied to voice change in order to compare differential development both between (males vs females; Tsimane vs North American; better vs worse condition) and within (voice vs height; fundamental frequency vs formant structure) populations. SUBJECTS AND METHODS: Fundamental and formant frequencies, as well as height and weight, were measured for 172 Tsimane males and females, aged 8-23. Participants were assigned to 'better' or 'worse' condition based on a median split of height-for-age and weight-for-age z-scores. RESULTS: Results support dramatic vocal changes in males. Peak voice change among Tsimane male adolescents occurs∼1 year later than in an age-matched North American sample. Achieved adult male voices are also higher in the Tsimane. Tsimane males in worse condition experience voice change more than 1 year later than Tsimane males in better condition. CONCLUSION: Voice change has a number of attractive features as a marker of male pubertal timing including its methodological and technical simplicity as well as its social salience to group members.

Fatty acid composition in the mature milk of Bolivian forager-horticulturalists: controlled comparisons with a US sample.

Breast milk fatty acid (FA) composition varies greatly among individual women, including in percentages of the long-chain polyunsaturated FAs (LCPUFA) 20:4n-6 (arachidonic acid, AA) and 22:6n-3 (docosahexaenoic acid, DHA), which are important for infant neurological development. It has been suggested that owing to wide variation in milk LCPUFA and low DHA in Western diets, standards of milk FA composition should be derived from populations consuming traditional diets. We collected breast milk samples from Tsimane women at varying lactational stages (6-82 weeks). The Tsimane are an indigenous, natural fertility, subsistence-level population living in Amazonia Bolivia. Tsimane samples were matched by lactational stage to samples from a US milk bank, and analysed concurrently for FA composition by gas-liquid chromatography. We compared milk FA composition between Tsimane (n = 35) and US (n = 35) mothers, focusing on differences in LCPUFA percentages that may be due to population-typical dietary patterns. Per total FAs, the percentages of AA, DHA, total n-3 and total n-6 LCPUFA were significantly higher among Tsimane mothers. Mean percentages of 18:2n-6 (linoleic acid) and trans FAs were significantly higher among US mothers. Tsimane mothers' higher milk n-3 and n-6 LCPUFA percentages may be due to their regular consumption of wild game and freshwater fish, as well as comparatively lower intakes of processed foods and oils that may interfere with LCPUFA synthesis.

Substantial but Misunderstood Human Sexual Dimorphism Results Mainly From Sexual Selection on Males and Natural Selection on Females.

Human sexual dimorphism has been widely misunderstood. A large literature has underestimated the effect of differences in body composition and the role of male contest competition for mates. It is often assumed that sexually dimorphic traits reflect a history of sexual selection, but natural selection frequently builds different phenotypes in males and females. The relatively small sex difference in stature (∼7%) and its decrease during human evolution have been widely presumed to indicate decreased male contest competition for mates. However, females likely increased in stature relative to males in order to successfully deliver large-brained neonates through a bipedally-adapted pelvis. Despite the relatively small differences in stature and body mass (∼16%), there are marked sex differences in body composition. Across multiple samples from groups with different nutrition, males typically have 36% more lean body mass, 65% more muscle mass, and 72% more arm muscle than women, yielding parallel sex differences in strength. These sex differences in muscle and strength are comparable to those seen in primates where sexual selection, arising from aggressive male mating competition, has produced high levels of dimorphism. Body fat percentage shows a reverse pattern, with females having ∼1.6 times more than males and depositing that fat in different body regions than males. We argue that these sex differences in adipose arise mainly from natural selection on women to accumulate neurodevelopmental resources.

Cognitive adaptations for gathering-related navigation in humans.

Current research increasingly suggests that spatial cognition in humans is accomplished by many specialized mechanisms, each designed to solve a particular adaptive problem. A major adaptive problem for our hominin ancestors, particularly females, was the need to efficiently gather immobile foods which could vary greatly in quality, quantity, spatial location and temporal availability. We propose a cognitive model of a navigational gathering adaptation in humans and test its predictions in samples from the US and Japan. Our results are uniformly supportive: the human mind appears equipped with a navigational gathering adaptation that encodes the location of gatherable foods into spatial memory. This mechanism appears to be chronically active in women and activated under explicit motivation in men.

Voice correlates of mating success in men: examining "contests" versus "mate choice" modes of sexual selection.

Men's copulatory success can often be predicted by measuring traits involved in male contests and female choice. Previous research has demonstrated relationships between one such vocal trait in men, mean fundamental frequency (F(0)), and the outcomes and indicators of sexual success with women. The present study investigated the role of another vocal parameter, F(0) variation (the within-subject SD in F(0) across the utterance, F(0)-SD), in predicting men's reported number of female sexual partners in the last year. Male participants (N = 111) competed with another man for a date with a woman. Recorded interactions with the competitor ("competitive recording") and the woman ("courtship recording") were analyzed for five non-linguistic vocal parameters: F(0)-SD, mean F(0), intensity, duration, and formant dispersion (D( f ), an acoustic correlate of vocal tract length), as well as dominant and attractive linguistic content. After controlling for age and attitudes toward uncommitted sex (SOI), lower F(0)-SD (i.e., a more monotone voice) and more dominant linguistic content were strong predictors of the number of past-year sexual partners, whereas mean F(0) and D( f ) did not significantly predict past-year partners. These contrasts have implications for the relative importance of male contests and female choice in shaping men's mating success and hence the origins and maintenance of sexually dimorphic traits in humans.

Does Nubility Indicate More Than High Reproductive Value? Nubile Primiparas' Pregnancy Outcomes in Evolutionary Perspective.

The idea that human males are most strongly attracted to traits that peak in women in the nubile age group raises the question of how well women in that age group contend with the potential hazards of a first pregnancy. Using data for 1.7 million first births from 1990 U.S. natality and mortality records, we compared outcomes for women with first births (primiparas) aged 16-20 years (when first births typically occur in forager and subsistence groups) with those aged 21-25 years. The younger primiparas had a much lower risk of potentially life-threatening complications of labor and delivery and, when evolutionarily novel risk factors were controlled, fetuses which were significantly more likely to survive despite lower birth weights. Thus, nubile primiparas were more likely to have a successful reproductive outcome defined in an evolutionarily relevant way (an infant of normal birth weight and gestation, surviving to one year, and delivered without a medically necessary cesarean delivery). This suggests that prior to the widespread availability of surgical deliveries, men who mated with women in the nubile age group would have reaped the benefit of having a reproductive partner more likely to have a successful first pregnancy.

Male Mating Expectations in Brazilian and American Samples.

This study aims to investigate assortative mating based on mate value from male perspective. Male participants (132 Brazilian and 106 American) evaluated hypothetical "stimulus" males described in terms of physical attractiveness, social skills, and social status (each varied in high or low levels). Participants rated each stimulus and each stimulus' preferred mating partner on nine traits. The results showed that (1) positive assortative mating was expected in romantic relationships; (2) the stimulus ratings did not vary independently, suggesting that mate value is the result of the interaction of the characteristics of individuals; and (3) that participants expected physically attractive and healthier female partners to pair with high-status male stimuli. The American and Brazilian mating expectations were similar, minor differences indicate that Brazilian participants considered men with high levels of social skills to be more ambitious and intelligent; American participants expected men of high status to be healthier; Brazilians expect men of high status to have more attractive faces, while Americans expected these men to possess more attractive bodies; and Brazilian participants assigned more attractive bodies to men of lower status. These differences reflect the influence of economic and cultural factors on the local environment. The study contributes to the understanding of the construction of market value and reveals that male expectations are in line with human mating preferences. The investigation of mating expectations can be a rich approach to investigate socio-cultural aspects that are related to mating in different cultures.

Was facial width-to-height ratio subject to sexual selection pressures? A life course approach.

Sexual selection researchers have traditionally focused on adult sex differences; however, the schedule and pattern of sex-specific ontogeny can provide insights unobtainable from an exclusive focus on adults. Recently, it has been debated whether facial width-to-height ratio (fWHR; bi-zygomatic breadth divided by midface height) is a human secondary sexual characteristic (SSC). Here, we review current evidence, then address this debate using ontogenetic evidence, which has been under-explored in fWHR research. Facial measurements were collected from 3D surface images of males and females aged 3 to 40 (Study 1; US European-descent, n = 2449), and from 2D photographs of males and females aged 7 to 21 (Study 2; Bolivian Tsimane, n = 179), which were used to calculate three fWHR variants (which we call fWHRnasion, fWHRstomion, and fWHRbrow) and two other common facial masculinity ratios (facial width-to-lower-face-height ratio, fWHRlower, and cheekbone prominence). We test whether the observed pattern of facial development exhibits patterns indicative of SSCs, i.e., differential adolescent growth in either male or female facial morphology leading to an adult sex difference. Results showed that only fWHRlower exhibited both adult sex differences as well as the classic pattern of ontogeny for SSCs-greater lower-face growth in male adolescents relative to females. fWHRbrow was significantly wider among both pre- and post-pubertal males in the Bolivian Tsimane sample; post-hoc analyses revealed that the effect was driven by large sex differences in brow height, with females having higher placed brows than males across ages. In both samples, all fWHR measures were inversely associated with age; that is, human facial growth is characterized by greater relative elongation in the mid-face and lower face relative to facial width. This trend continues even into middle adulthood. BMI was also a positive predictor of most of the ratios across ages, with greater BMI associated with wider faces. Researchers collecting data on fWHR should target fWHRlower and fWHRbrow and should control for both age and BMI. Researchers should also compare ratio approaches with multivariate techniques, such as geometric morphometrics, to examine whether the latter have greater utility for understanding the evolution of facial sexual dimorphism.

Cross-Cultural and Cross-Organizational Evidence for an Evolved Hazing Motivation.

We report the first cross-cultural and cross-organizational evidence for an evolved hazing motivation. Using experiments performed in the United States, Japan, and among members of a hazing and a nonhazing organization, we demonstrate an invariant set of core hazing predictors. In particular, we show that the perception of near-term group benefits, which would have been ancestrally exploitable by new group members, substantially increases desired hazing severity in all samples. Results are discussed in light of human organizational psychology and the difficulty of reliably suppressing hazing behavior.

Do the Low WHRs and BMIs Judged Most Attractive Indicate Higher Fertility?

We examine the widely accepted view that very low waist-hip ratios and low body mass indices (BMIs) in women in well-nourished populations are judged attractive by men because these features reliably indicate superior fertility. In both subsistence and well-nourished populations, relevant studies of fertility do not support this view. Rather studies indicate lower fertility in women with anthropometric values associated with high attractiveness. Moreover, low maternal BMI predisposes to conditions that compromise infant survival. Consistent with these findings from the literature, new data from a large U.S. sample of women past reproductive age show that women with lower BMIs in the late teens had fewer live births, controlling for education, marital history, and race. They also had later menarche and earlier menopause compared with women with higher youth BMIs. In addition, data from the 2013 U.S. natality database show that mothers with lower prepregnancy BMIs have an increased risk of producing both low-birth-weight and preterm infants controlling for other relevant variables-conditions that would have adversely affected fitness over almost all of human evolution. Thus, a review of the relevant literature and three new tests fail to support the view that highly attractive women are more fertile.

Do the Low WHRs and BMIs Judged Most Attractive Indicate Better Health?

It is widely claimed that in well-nourished populations, very low female waist-hip ratios (WHRs) together with low body mass indices (BMIs) are judged attractive by men because these features reliably indicate superior health and fertility. However, studies show that mortality rates are higher in women with low BMIs than in women with average BMIs and are inversely related to BMI in subsistence populations. Measures of current health in women of reproductive age have not been similarly studied. We analyze large U.S. samples of reproductive-age women and show that controlling for other factors known to affect health, those with low BMIs (<20), WHRs, or waist/stature ratios did not have better health than those with values in the middle range, and there was no relationship between subsequent health outcomes and BMI in early adulthood. Lower self-reported BMIs were linked to poorer health and an increased risk of infection. However, based on recent U.S. natality data, primiparas with lower BMIs had a lower risk of an operative delivery and of gestational hypertension. Beyond these two parity-restricted effects, relevant studies and new tests fail to support the view that women with the very low BMIs and WHRs consistently judged attractive are generally healthier than women with average values; significant correlations were consistently in the opposite direction.

Spatial adaptations for plant foraging: women excel and calories count.

We present evidence for an evolved sexually dimorphic adaptation that activates spatial memory and navigation skills in response to fruits, vegetables and other traditionally gatherable sessile food resources. In spite of extensive evidence for a male advantage on a wide variety of navigational tasks, we demonstrate that a simple but ecologically important shift in content can reverse this sex difference. This effect is predicted by and consistent with the theory that a sexual division in ancestral foraging labour selected for gathering-specific spatial mechanisms, some of which are sexually differentiated. The hypothesis that gathering-specific spatial adaptations exist in the human mind is further supported by our finding that spatial memory is preferentially engaged for resources with higher nutritional quality (e.g. caloric density). This result strongly suggests that the underlying mechanisms evolved in part as adaptations for efficient foraging. Together, these results demonstrate that human spatial cognition is content sensitive, domain specific and designed by natural selection to mesh with important regularities of the ancestral world.

Why Go There? Evolution of Mobility and Spatial Cognition in Women and Men : An Introduction to the Special Issue.

Males in many non-monogamous species have larger ranges than females do, a sex difference that has been well documented for decades and seems to be an aspect of male mating competition. Until recently, parallel data for humans have been mostly anecdotal and qualitative, but this is now changing as human behavioral ecologists turn their attention to matters of individual mobility. Sex differences in spatial cognition were among the first accepted psychological sex differences and, like differences in ranging behavior, are documented for a growing set of species. This special issue is dedicated to exploring the possible adaptive links between these cognitive and ranging traits. Multiple hypotheses, at various levels of analysis, are considered. At the functional (ultimate) level, a mating-competition hypothesis suggests that range expansion may augment mating opportunities, and a fertility-and-parental-care hypothesis suggests that range contraction may facilitate offspring provisioning. At a more mechanistic (proximate) level, differences in cue availability may support or inhibit particular sex-specific navigation strategies, and spatial anxiety may usefully inhibit travel that would not justify its costs. Studies in four different cultures-Twe, Tsimane, Yucatec Maya, and Faroese-as well as an experimental study using virtual reality tools are the venue for testing these hypotheses. Our hope is to stimulate more research on the evolutionary and developmental processes responsible for this suite of linked behavioral and cognitive traits.

Facial Width-To-Height Ratio (fWHR) Is Not Associated with Adolescent Testosterone Levels.

Facial width-to-height ratio (fWHR) has been proposed as a sexually dimorphic signal in humans that develops under the influence of pubertal testosterone (T); however, no studies have examined the association between fWHR and T during the phase in which facial growth is canalized--adolescence. In a sample of adolescent Tsimane males, we evaluate the relationship between T, known T-derived traits (i.e. strength and voice pitch), and craniofacial measurements. If fWHR variation derives from T's effect on craniofacial growth during adolescence, several predictions should be supported: 1) fWHR should increase with age as T increases, 2) fWHR should reflect adolescent T (rather than adult T per se), 3) fWHR should exhibit velocity changes during adolescence in parallel with the pubertal spurt in T, 4) fWHR should correlate with T after controlling for age and other potential confounds, and 5) fWHR should show strong associations with other T-derived traits. Only prediction 4 was observed. Additionally, we examined three alternative facial masculinity ratios: facial width/lower face height, cheekbone prominence, and facial width/full face height. In contrast to fWHR, all three alternative measures show a strong age-related trend and are associated with both T and T-dependent traits. Overall, our results question the status of fWHR as a sexually-selected signal of pubertal T and T-linked traits.

No Sex or Age Difference in Dead-Reckoning Ability among Tsimane Forager-Horticulturalists.

Sex differences in reproductive strategy and the sexual division of labor resulted in selection for and maintenance of sexual dimorphism across a wide range of characteristics, including body size, hormonal physiology, behavior, and perhaps spatial abilities. In laboratory tasks among undergraduates there is a general male advantage for navigational and mental-rotation tasks, whereas studies find female advantage for remembering item locations in complex arrays and the locations of plant foods. Adaptive explanations of sex differences in these spatial abilities have focused on patterns of differential mate search and routine participation in distinct subsistence behaviors. The few studies to date of spatial ability in nonindustrial populations practicing subsistence lifestyles, or across a wider age range, find inconsistent results. Here we examine sex- and age-based variation in one kind of spatial ability related to navigation, dead-reckoning, among Tsimane forager horticulturalists living in lowland Bolivia. Seventy-three participants (38 male) aged 6-82 years pointed a handheld global positioning system (GPS) unit toward the two nearest communities and the more distant market town. We find no evidence of sex differences in dead reckoning (p = 0.47), nor do we find any evidence of age-related decline in dead-reckoning accuracy (p = 0.28). Participants were significantly more accurate at pointing toward the market town than toward the two nearest villages despite its being significantly farther away than the two nearest communities. Although Tsimane do show sexual dimorphism in foraging tasks, Tsimane women have extensive daily and lifetime travel, and the local environment lacks directional cues that typically enhance male navigation. This study raises the possibility that greater similarity in mobility patterns because of overlapping subsistence strategies and activities may result in convergence of some male and female navigation abilities.