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.

Hearing Prosocial Stories Increases Hadza Hunter-Gatherers' Generosity in an Economic Game.

Folk stories featuring prosocial content are ubiquitous across cultures. One explanation for the ubiquity of such stories is that stories teach people about the local socioecology, including norms of prosociality, and stories featuring prosocial content may increase generosity in listeners. We tested this hypothesis in a sample of 185 Hadza hunter-gatherers. We read participants a story in which the main character either swims with another person (control story) or rescues him from drowning (prosocial story). After hearing the story, participants played a dictator game with dried meat sticks and then were given a recall test of facts presented in the story. There was moderate evidence for a small effect of the prosocial story: participants who heard the prosocial story gave an estimated 0.22 [90% HDI: -0.12-0.57] more meat sticks than those who heard the control story. However, the association between generosity and sex, marital status, and region of residence was stronger; men gave more than women, unmarried participants gave more than married participants, and participants living in a region with more exposure to markets gave more than participants living further from markets. There was no evidence that the prosocial story was more easily recalled than the control story. These results provide some support for the hypothesis that prosocial stories can increase prosociality in listeners, though the effect of hearing a single story is small.

Hadza hunter-gatherers with greater exposure to other cultures share more with generous campmates.

Humans are motivated to compete for access to valuable social partners, which is a function of their willingness to share and ability to generate resources. However, relative preferences for each trait should be responsive to socioecological conditions. Here, we test the flexibility of partner choice psychology among Hadza hunter-gatherers of Tanzania. Ninety-two Hadza ranked their campmates on generosity and foraging ability and then shared resources with those campmates. We found Hadza with greater exposure to other cultures shared more with campmates ranked higher on generosity, whereas Hadza with lower exposure showed a smaller preference for sharing with generous campmates. This moderating effect was specific to generosity-regardless of exposure, Hadza showed only a small preference for sharing with better foragers. We argue this difference in preferences is due to high exposure Hadza having more experience cooperating with others in the absence of strong norms of sharing, and thus are exposed to greater variance in willingness to cooperate among potential partners increasing the benefits of choosing partners based on generosity. As such, participants place a greater emphasis on choosing more generous partners, highlighting the flexibility of partner preferences.

Evidence against the "anomalous-is-bad" stereotype in Hadza hunter gatherers.

People have an "anomalous-is-bad" stereotype whereby they make negative inferences about the moral character of people with craniofacial anomalies like scars. This stereotype is hypothesized to be a byproduct of adaptations for avoiding pathogens. However, evidence for the anomalous-is-bad stereotype comes from studies of European and North American populations; the byproduct hypothesis would predict universality of the stereotype. We presented 123 Hadza across ten camps pairs of morphed Hadza faces-each with one face altered to include a scar-and asked who they expected to be more moral and a better forager. Hadza with minimal exposure to other cultures chose at chance for both questions. Hadza with greater exposure to other cultures, however, expected the scarred face to be less moral and a better forager. These results suggest the anomalous-is-bad stereotype may be culturally shared or learned erroneously through associations with population-level differences, providing evidence against a universal pathogen avoidance byproduct hypothesis.

The evolution of human cooperation.

Darwin viewed cooperation as a perplexing challenge to his theory of natural selection. Natural selection generally favors the evolution of behaviors that enhance the fitness of individuals. Cooperative behavior, which increases the fitness of a recipient at the expense of the donor, contradicts this logic. William D. Hamilton helped to solve the puzzle when he showed that cooperation can evolve if cooperators direct benefits selectively to other cooperators (i.e. assortment). Kinship, group selection and the previous behavior of social partners all provide mechanisms for assortment (Figure 1), and kin selection and reciprocal altruism are the foundation of the kinds of cooperative behavior observed in many animals. Humans also bias cooperation in favor of kin and reciprocating partners, but the scope, scale, and variability of human cooperation greatly exceed that of other animals. Here, we introduce derived features of human cooperation in the context in which they originally evolved, and discuss the processes that may have shaped the evolution of our remarkable capacity for cooperation. We argue that culturally-evolved norms that specify how people should behave provide an evolutionarily novel mechanism for assortment, and play an important role in sustaining derived properties of cooperation in human groups.

Moralizing gods, impartiality and religious parochialism across 15 societies.

The emergence of large-scale cooperation during the Holocene remains a central problem in the evolutionary literature. One hypothesis points to culturally evolved beliefs in punishing, interventionist gods that facilitate the extension of cooperative behaviour toward geographically distant co-religionists. Furthermore, another hypothesis points to such mechanisms being constrained to the religious ingroup, possibly at the expense of religious outgroups. To test these hypotheses, we administered two behavioural experiments and a set of interviews to a sample of 2228 participants from 15 diverse populations. These populations included foragers, pastoralists, horticulturalists, and wage labourers, practicing Buddhism, Christianity, and Hinduism, but also forms of animism and ancestor worship. Using the Random Allocation Game (RAG) and the Dictator Game (DG) in which individuals allocated money between themselves, local and geographically distant co-religionists, and religious outgroups, we found that higher ratings of gods as monitoring and punishing predicted decreased local favouritism (RAGs) and increased resource-sharing with distant co-religionists (DGs). The effects of punishing and monitoring gods on outgroup allocations revealed between-site variability, suggesting that in the absence of intergroup hostility, moralizing gods may be implicated in cooperative behaviour toward outgroups. These results provide support for the hypothesis that beliefs in monitoring and punitive gods help expand the circle of sustainable social interaction, and open questions about the treatment of religious outgroups.

Hunter-Gatherers Maintain Assortativity in Cooperation despite High Levels of Residential Change and Mixing.

Widespread cooperation is a defining feature of human societies from hunter-gatherer bands to nation states [1, 2], but explaining its evolution remains a challenge. Although positive assortment of cooperators is recognized as a basic requirement for the evolution of cooperation, the mechanisms governing assortment are debated. Moreover, the social structure of modern hunter-gatherers, characterized by high mobility, residential mixing, and low genetic relatedness [3], undermines assortment and adds to the puzzle of how cooperation evolved. Here, we analyze four years of data (2010, 2013, 2014, 2016) tracking residence and levels of cooperation elicited from a public goods game in Hadza hunter-gatherers of Tanzania. Data were collected from 56 camps, comprising 383 unique individuals, 137 of whom we have data for two or more years. Despite significant residential mixing, we observe a robust pattern of assortment that is necessary for cooperation to evolve; in every year, Hadza camps exhibit high between-camp and low within-camp variation in cooperation. We find little evidence that cooperative behavior within individuals is stable over time or that similarity in cooperation between dyads predicts their future cohabitation. Both sets of findings are inconsistent with models that assume stable cooperative and selfish types, including partner choice models. Consistent with social norms, culture, and reciprocity theories, the strongest predictor of an individual's level of cooperation is the mean cooperation of their current campmates. These findings underscore the adaptive nature of human cooperation-particularly its responsiveness to social contexts-as a feature that is important in generating the assortment necessary for cooperation to evolve.

Evidence from hunter-gatherer and subsistence agricultural populations for the universality of contagion sensitivity.

The phenomenon of magical contagion - the unobserved passage of properties between entities that come into physical contact - was described by anthropologists over a century ago, yet questions remain about its origin, function, and universality. Contagion sensitivity, along with the emotion of disgust, has been proposed to be part of a biologically-evolved system designed to reduce exposure to pathogens by increasing the avoidance of "contaminated" objects. Yet this phenomenon has not been studied using systematic psychological comparison outside of industrialized populations. Here we document contagion sensitivity in two culturally, geographically, and economically distinct populations with little exposure to Western biomedicine and formal education: the Hadza hunter-gatherers of Tanzania and Tannese subsistence-agriculturalists of Vanuatu. In both populations, a majority of individuals rejected familiar and palatable foods when contaminating items touched the food but were subsequently removed. The Tannese children in our study showed a similar response, consistent with previous research with Western children. Our data support the proposal that contagion sensitivity is universal in human populations.

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.

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.

Winners, losers, and posers: The effect of power poses on testosterone and risk-taking following competition.

A contribution to a special issue on Hormones and Human Competition. The effect of postural power displays (i.e. power poses) on hormone levels and decision-making has recently been challenged. While Carney et al. (2010) found that holding brief postural displays of power leads to increased testosterone, decreased cortisol and greater economic risk taking, this failed to replicate in a recent high-powered study (Ranehill et al. 2015). It has been put forward that subtle differences in social context may account for the differences in results. Power displays naturally occur within the context of competitions, as do changes in hormones, and researchers have yet to examine the effects of poses within this ecologically relevant context. Using a large sample of 247 male participants, natural winners and losers of a physical competition were randomly assigned to hold a low, neutral or high-power postural display. We found no main effect of pose type on testosterone, cortisol, risk or feelings of power. Winners assigned to a high-power pose had a relative, albeit small, rise in testosterone compared to winners who held neutral or low-power poses. For losers, we found little evidence that high-power poses lead to increased testosterone relative to those holding neutral or low-powered poses. If anything, the reverse was observed - losers had a reduction in testosterone after holding high-power poses. To the extent that changes in testosterone modulate social behaviors adaptively, it is possible that the relative reduction in testosterone observed in losers taking high-powered poses is designed to inhibit further "winner-like" behavior that could result in continued defeat and harm. Still, effects were small, multiple comparisons were made, and the results ran counter to our predictions. We thus treat these conclusions as preliminary.

Detecting affiliation in colaughter across 24 societies.

Laughter is a nonverbal vocal expression that often communicates positive affect and cooperative intent in humans. Temporally coincident laughter occurring within groups is a potentially rich cue of affiliation to overhearers. We examined listeners' judgments of affiliation based on brief, decontextualized instances of colaughter between either established friends or recently acquainted strangers. In a sample of 966 participants from 24 societies, people reliably distinguished friends from strangers with an accuracy of 53-67%. Acoustic analyses of the individual laughter segments revealed that, across cultures, listeners' judgments were consistently predicted by voicing dynamics, suggesting perceptual sensitivity to emotionally triggered spontaneous production. Colaughter affords rapid and accurate appraisals of affiliation that transcend cultural and linguistic boundaries, and may constitute a universal means of signaling cooperative relationships.

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.

Hadza Color Terms Are Sparse, Diverse, and Distributed, and Presage the Universal Color Categories Found in Other World Languages.

In our empirical and theoretical study of color naming among the Hadza, a Tanzanian hunter-gatherer group, we show that Hadza color naming is sparse (the color appearance of many stimulus tiles was not named), diverse (there was little consensus in the terms for the color appearance of most tiles), and distributed (the universal color categories of world languages are revealed in nascent form within the Hadza language community, when we analyze the patterns of how individual Hadza deploy color terms). Using our Hadza data set, Witzel shows an association between two measures of color naming performance and the chroma of the stimuli. His prediction of which colored tiles will be named with what level of consensus, while interesting, does not alter the validity of our conclusions.

Hadza hunter-gatherer men do not have more masculine digit ratios (2D:4D).

OBJECTIVES: The ratio between the length of the second and the length of the fourth digit (2D:4D) is sexually dimorphic such that males of many species possess a lower ratio than females, particularly in the right hand. Still, men and women often exhibit overlapping 2D:4D ranges and the ratio is highly variable between populations. In order to further explore populational variability, we chose to analyze 2D:4D in the Hadza, a population of hunter-gatherers living in Tanzania. MATERIALS AND METHODS: Data were collected separately by two researchers over the course of three years (1998, 2001, 2006) from 152 adult participants (male: n = 76, female: n = 76). Independent samples t-tests were used to explore sex differences, paired samples t-tests were used to explore directional effects within each sex, and linear regression and one-way ANOVA were used to test possible age effects. RESULTS: In none of the years, or pooled (n = 152), did we find evidence that adult men have a lower 2D:4D than adult women. If anything, the data suggest that women in this population have a significantly lower right hand 2D:4D than men (P < 0.001, d = 0.57). In contrast, left hand 2D:4D did not exhibit a sex difference (P = 0.862, d = 0.03). DISCUSSION: These findings challenge the current view that lower 2D:4D in men is a uniform characteristic of our species. Cross-populational variance in 2D:4D may be related to known patterns of hormonal variation resulting from both genetic and environmental mechanisms, though this relationship merits further investigation.

Face adaptation in an isolated population of African hunter-gatherers: Exposure influences perception of other-ethnicity faces more than own-ethnicity faces.

Previous experiments have demonstrated that exposure to faces can change the perception of normality in new faces, such that faces similar to those at exposure appear more normal. Here we examined how experience influences adaptation effects in African Hadza hunter-gatherers, who have limited experience with White faces. We exposed participants to sets of either Hadza or White European faces that were manipulated to possess either wide-spaced or narrow-spaced eyes. We collected normality judgments both pre-exposure and post-exposure by showing pairs of images, one with wide-spaced and one with narrow-spaced eyes. Examining the difference between the pre-exposure and post-exposure judgments revealed that participants selected an increased number of images that were congruent with the faces to which they had been exposed. The change in normality judgments was strongest for White faces, suggesting that representations of White ethnicity faces are more malleable and less robust to adaptation, potentially because of the decreased experience that individuals had with them. A second experiment using the same test stimuli with a sample of White participants revealed equivalent adaptation effects for both Hadza and White faces. These data highlight the role of experience on the high-level visual adaptation of faces.

Hunter-Gatherer Color Naming Provides New Insight into the Evolution of Color Terms.

Most people name the myriad colors in the environment using between two and about a dozen color terms, with great variation within and between languages. Investigators generally agree that color lexicons evolve from fewer terms to more terms, as technology advances and color communication becomes increasingly important. However, little is understood about the color naming systems at the least technologically advanced end of the continuum. The Hadza people of Tanzania are nomadic hunter-gatherers who live a subsistence lifestyle that was common before the advent of agriculture (see Supplemental Experimental Procedures, section I;), suggesting that the Hadzane language should be at an early stage of color lexicon evolution. When Hadza, Somali, and US informants named 23 color samples, Hadza informants named only the black, white, and red samples with perfect consensus. Otherwise, they used low-consensus terms or responded "don't know." However, even low-consensus color terms grouped test colors into lexical categories that aligned with those found in other world languages. Furthermore, information-theoretic analysis showed that color communication efficiency within the Hadza, Somali, and US language communities falls on the same continuum as other world languages. Thus, the structure of color categories is in place in Hadzane, even though words for many of the categories are not in general use. These results suggest that even very simple color lexicons include precursors of many color categories but that these categories are initially represented in a diverse and distributed fashion.

Salivary testosterone change following monetary wins and losses predicts future financial risk-taking.

While baseline testosterone has recently been implicated in risk-taking in men, less is known about the effects of changing levels of testosterone on financial risk. Here we attempt to influence testosterone in men by having them win or lose money in a chance-based competition against another male opponent. We employ two treatments where we vary the amount of money at stake so that we can directly compare winners to losers who earn the same amount, thereby abstracting from income effects. We find that men who experience a greater increase in bioactive testosterone take on more risk, an association that remains when controlling for whether the participant won the competition. In fact, whether subjects won the competition did not predict future risk. These results suggest that testosterone change, and thus individual differences in testosterone reactivity, rather than the act of winning or losing, influence financial risk-taking.

Social networks and cooperation in hunter-gatherers.

Social networks show striking structural regularities, and both theory and evidence suggest that networks may have facilitated the development of large-scale cooperation in humans. Here, we characterize the social networks of the Hadza, a population of hunter-gatherers in Tanzania. We show that Hadza networks have important properties also seen in modernized social networks, including a skewed degree distribution, degree assortativity, transitivity, reciprocity, geographic decay and homophily. We demonstrate that Hadza camps exhibit high between-group and low within-group variation in public goods game donations. Network ties are also more likely between people who give the same amount, and the similarity in cooperative behaviour extends up to two degrees of separation. Social distance appears to be as important as genetic relatedness and physical proximity in explaining assortativity in cooperation. Our results suggest that certain elements of social network structure may have been present at an early point in human history. Also, early humans may have formed ties with both kin and non-kin, based in part on their tendency to cooperate. Social networks may thus have contributed to the emergence of cooperation.

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 men's 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 men's 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.