Exploring Adaptive Phenotypes for the Human Calcium-Sensing Receptor Polymorphism R990G.

Rainforest hunter-gatherers from Southeast Asia are characterized by specific morphological features including a particularly dark skin color (D), short stature (S), woolly hair (W), and the presence of steatopygia (S)-fat accumulation localized in the hips (DSWS phenotype). Based on previous evidence in the Andamanese population, we first characterized signatures of adaptive natural selection around the calcium-sensing receptor gene in Southeast Asian rainforest groups presenting the DSWS phenotype and identified the R990G substitution (rs1042636) as a putative adaptive variant for experimental follow-up. Although the calcium-sensing receptor has a critical role in calcium homeostasis by directly regulating the parathyroid hormone secretion, it is expressed in different tissues and has been described to be involved in many biological functions. Previous works have also characterized the R990G substitution as an activating polymorphism of the calcium-sensing receptor associated with hypocalcemia. Therefore, we generated a knock-in mouse for this substitution and investigated organismal phenotypes that could have become adaptive in rainforest hunter-gatherers from Southeast Asia. Interestingly, we found that mouse homozygous for the derived allele show not only lower serum calcium concentration but also greater body weight and fat accumulation, probably because of enhanced preadipocyte differentiation and lipolysis impairment resulting from the calcium-sensing receptor activation mediated by R990G. We speculate that such differential features in humans could have facilitated the survival of hunter-gatherer groups during periods of nutritional stress in the challenging conditions of the Southeast Asian tropical rainforests.

Agta hunter-gatherer oral microbiomes are shaped by contact network structure.

Here we investigate the effects of extensive sociality and mobility on the oral microbiome of 138 Agta hunter-gatherers from the Philippines. Our comparisons of microbiome composition showed that the Agta are more similar to Central African BaYaka hunter-gatherers than to neighbouring farmers. We also defined the Agta social microbiome as a set of 137 oral bacteria (only 7% of 1980 amplicon sequence variants) significantly influenced by social contact (quantified through wireless sensors of short-range interactions). We show that large interaction networks including strong links between close kin, spouses and even unrelated friends can significantly predict bacterial transmission networks across Agta camps. Finally, we show that more central individuals to social networks are also bacterial supersharers. We conclude that hunter-gatherer social microbiomes are predominantly pathogenic and were shaped by evolutionary tradeoffs between extensive sociality and disease spread.

Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Understanding hunter-gatherer cultural evolution needs network thinking.

Hunter-gatherers past and present live in complex societies, and the structure of these can be assessed using social networks. We outline how the integration of new evidence from cultural evolution experiments, computer simulations, ethnography, and archaeology open new research horizons to understand the role of social networks in cultural evolution.

Population interconnectivity over the past 120,000 years explains distribution and diversity of Central African hunter-gatherers.

The evolutionary history of African hunter-gatherers holds key insights into modern human diversity. Here, we combine ethnographic and genetic data on Central African hunter-gatherers (CAHG) to show that their current distribution and density are explained by ecology rather than by a displacement to marginal habitats due to recent farming expansions, as commonly assumed. We also estimate the range of hunter-gatherer presence across Central Africa over the past 120,000 years using paleoclimatic reconstructions, which were statistically validated by our newly compiled dataset of dated archaeological sites. Finally, we show that genomic estimates of divergence times between CAHG groups match our ecological estimates of periods favoring population splits, and that recoveries of connectivity would have facilitated subsequent gene flow. Our results reveal that CAHG stem from a deep history of partially connected populations. This form of sociality allowed the coexistence of relatively large effective population sizes and local differentiation, with important implications for the evolution of genetic and cultural diversity in Homo sapiens.

The origins of human cumulative culture: from the foraging niche to collective intelligence.

Various studies have investigated cognitive mechanisms underlying culture in humans and other great apes. However, the adaptive reasons for the evolution of uniquely sophisticated cumulative culture in our species remain unclear. We propose that the cultural capabilities of humans are the evolutionary result of a stepwise transition from the ape-like lifestyle of earlier hominins to the foraging niche still observed in extant hunter-gatherers. Recent ethnographic, archaeological and genetic studies have provided compelling evidence that the components of the foraging niche (social egalitarianism, sexual and social division of labour, extensive co-residence and cooperation with unrelated individuals, multilocality, fluid sociality and high between-camp mobility) engendered a unique multilevel social structure where the cognitive mechanisms underlying cultural evolution (high-fidelity transmission, innovation, teaching, recombination, ratcheting) evolved as adaptations. Therefore, multilevel sociality underlies a 'social ratchet' or irreversible task specialization splitting the burden of cultural knowledge across individuals, which may explain why human collective intelligence is uniquely able to produce sophisticated cumulative culture. The foraging niche perspective may explain why a complex gene-culture dual inheritance system evolved uniquely in humans and interprets the cultural, morphological and genetic origins of Homo sapiens as a process of recombination of innovations appearing in differentiated but interconnected populations. This article is part of a discussion meeting issue 'The emergence of collective knowledge and cumulative culture in animals, humans and machines'.

Relatedness within and between Agta residential groups.

Theoretical models relating to the evolution of human behaviour usually make assumptions about the kinship structure of social groups. Since humans were hunter-gatherers for most of our evolutionary history, data on the composition of contemporary hunter-gatherer groups has long been used to inform these models. Although several papers have taken a broad view of hunter-gatherer social organisation, it is also useful to explore data from single populations in more depth. Here, we describe patterns of relatedness among the Palanan Agta, hunter-gatherers from the northern Philippines. Across 271 adults, mean relatedness to adults across the population is r = 0.01 and to adult campmates is r = 0.074, estimates that are similar to those seen in other hunter-gatherers. We also report the distribution of kin across camps, relatedness and age differences between spouses, and the degree of shared reproductive interest between camp mates, a measure that incorporates affinal kinship. For both this this measure (s) and standard relatedness (r), we see no major age or sex differences in the relatedness of adults to their campmates, conditions that may reduce the potential for conflicts of interest within social groups.

Multilevel Organisation of Animal Sociality.

Multilevel societies (MLSs), stable nuclear social units within a larger collective encompassing multiple nested social levels, occur in several mammalian lineages. Their architectural complexity and size impose specific demands on their members requiring adaptive solutions in multiple domains. The functional significance of MLSs lies in their members being equipped to reap the benefits of multiple group sizes. Here, we propose a unifying terminology and operational definition of MLS. To identify new avenues for integrative research, we synthesise current literature on the selective pressures underlying the evolution of MLSs and their implications for cognition, intersexual conflict, and sexual selection. Mapping the drivers and consequences of MLS provides a reference point for the social evolution of many taxa, including our own species.

Global WEIRDing: transitions in wild plant knowledge and treatment preferences in Congo hunter-gatherers.

Cultures around the world are converging as populations become more connected. On the one hand this increased connectedness can promote the recombination of existing cultural practices to generate new ones, but on the other it may lead to the replacement of traditional practices and global WEIRDing. Here we examine the process and causes of changes in cultural traits concerning wild plant knowledge in Mbendjele BaYaka hunter-gatherers from Congo. Our results show that the BaYaka who were born in town reported knowing and using fewer plants than the BaYaka who were born in forest camps. Plant uses lost in the town-born BaYaka related to medicine. Unlike the forest-born participants, the town-born BaYaka preferred Western medicine over traditional practices, suggesting that the observed decline of plant knowledge and use is the result of replacement of cultural practices with the new products of cumulative culture.

Development of social learning and play in BaYaka hunter-gatherers of Congo.

High-fidelity transmission of information through imitation and teaching has been proposed as necessary for cumulative cultural evolution. Yet, it is unclear when and for which knowledge domains children employ different social learning processes. This paper explores the development of social learning processes and play in BaYaka hunter-gatherer children by analysing video recordings and time budgets of children from early infancy to adolescence. From infancy to early childhood, hunter-gatherer children learn mainly by imitating and observing others' activities. From early childhood, learning occurs mainly in playgroups and through practice. Throughout childhood boys engage in play more often than girls whereas girls start foraging wild plants from early childhood and spend more time in domestic activities and childcare. Sex differences in play reflect the emergence of sexual division of labour and the play-work transition occurring earlier for girls. Consistent with theoretical models, teaching occurs for skills/knowledge that cannot be transmitted with high fidelity through other social learning processes such as the acquisition of abstract information e.g. social norms. Whereas, observational and imitative learning occur for the transmission of visually transparent skills such as tool use, foraging, and cooking. These results suggest that coevolutionary relationships between human sociality, language and teaching have likely been fundamental in the emergence of human cumulative culture.

Engagement in agricultural work is associated with reduced leisure time among Agta hunter-gatherers.

A long-standing hypothesis suggests that the transition from hunting and gathering to agriculture results in people working harder, spending more time engaged in subsistence activities and having less leisure time1,2. However, tests of this hypothesis are obscured by comparing between populations that vary in ecology and social organization, as well as subsistence3-6. Here we test this hypothesis by examining adult time allocation among the Agta-a population of small-scale hunter-gatherers from the northern Philippines who are increasingly engaged in agriculture and other non-foraging work. We find that individuals in camps engaging more in non-foraging work spend more time involved in out-of-camp work and have substantially less leisure time. This difference is largely driven by changes in the time allocation of women, who spend substantially more time engaged in out-of-camp work in more agricultural camps. Our results support the hypothesis that hunting and gathering allows a significant amount of leisure time, and that this is lost as communities adopt small-scale agriculture.

Why so many Agta boys? Explaining 'extreme' sex ratios in Philippine foragers.

Male-biased sex ratios have been observed in multiple small-scale societies. Although intentional and systematic female-biased mortality has been posited as an explanation, there is often a lack of ethnographic evidence of systematic female neglect and/or infanticide. The Agta, a foraging population from the Philippines, have a skewed sex ratio of 1.29 (129 males per 100 females) aged 15 years or under. We hypothesised that this skew was not caused by greater female deaths, but due to an adaptive response, where more males were produced at birth in reaction to high male-biased extrinsic mortality. To test this hypothesis we utilise census, childcare and mortality data from 915 Agta. The Agta's sex ratio is significantly male-biased in the <1 (n = 48, 2:1) and 1-5 year (n = 170, 1.39:1) age cohorts; however, we find no evidence of systematic female neglect in patterns of childcare. Furthermore, the sex ratio decreases over cohorts, becoming balanced by the end of the juvenile period, owing to significantly higher male mortality. Taken together, these results are not supportive of female infanticide or neglect, and instead suggest an adaptive mechanism, acting in utero as a response to male-biased juvenile mortality, following Fisherian principles of equalising parental investment.

Speech, stone tool-making and the evolution of language.

The 'technological hypothesis' proposes that gestural language evolved in early hominins to enable the cultural transmission of stone tool-making skills, with speech appearing later in response to the complex lithic industries of more recent hominins. However, no flintknapping study has assessed the efficiency of speech alone (unassisted by gesture) as a tool-making transmission aid. Here we show that subjects instructed by speech alone underperform in stone tool-making experiments in comparison to subjects instructed through either gesture alone or 'full language' (gesture plus speech), and also report lower satisfaction with their received instruction. The results provide evidence that gesture was likely to be selected over speech as a teaching aid in the earliest hominin tool-makers; that speech could not have replaced gesturing as a tool-making teaching aid in later hominins, possibly explaining the functional retention of gesturing in the full language of modern humans; and that speech may have evolved for reasons unrelated to tool-making. We conclude that speech is unlikely to have evolved as tool-making teaching aid superior to gesture, as claimed by the technological hypothesis, and therefore alternative views should be considered. For example, gestural language may have evolved to enable tool-making in earlier hominins, while speech may have later emerged as a response to increased trade and more complex inter- and intra-group interactions in Middle Pleistocene ancestors of Neanderthals and Homo sapiens; or gesture and speech may have evolved in parallel rather than in sequence.

Universality Without Uniformity: A Culturally Inclusive Approach to Sensitive Responsiveness in Infant Caregiving.

Do caregivers in non-Western communities adapt their behaviors to the needs of infants? This question reflects one of the most long-standing debates on the universality versus culture-specificity of caregiver-infant interactions in general and sensitive responsiveness to infants in particular. In this article, an integration of both points of view is presented, based on the theoretical origins of the sensitive responsiveness construct combined with the ethnographic literature on caregivers and infants in different parts of the world. This integration advocates universality without uniformity, and calls for multidisciplinary collaborations to investigate the complexities and nuances of caregiver-infant interactions in different cultures. Salient issues are illustrated with observations of infants (ages 7-31 months) in Mali, the Republic of Congo, and the Philippines.

Disentangling Immediate Adaptive Introgression from Selection on Standing Introgressed Variation in Humans.

Recent studies have reported evidence suggesting that portions of contemporary human genomes introgressed from archaic hominin populations went to high frequencies due to positive selection. However, no study to date has specifically addressed the postintrogression population dynamics of these putative cases of adaptive introgression. Here, for the first time, we specifically define cases of immediate adaptive introgression (iAI) in which archaic haplotypes rose to high frequencies in humans as a result of a selective sweep that occurred shortly after the introgression event. We define these cases as distinct from instances of selection on standing introgressed variation (SI), in which an introgressed haplotype initially segregated neutrally and subsequently underwent positive selection. Using a geographically diverse data set, we report novel cases of selection on introgressed variation in living humans and shortlist among these cases those whose selective sweeps are more consistent with having been the product of iAI rather than SI. Many of these novel inferred iAI haplotypes have potential biological relevance, including three that contain immune-related genes in West Siberians, South Asians, and West Eurasians. Overall, our results suggest that iAI may not represent the full picture of positive selection on archaically introgressed haplotypes in humans and that more work needs to be done to analyze the role of SI in the archaic introgression landscape of living humans.

Hunter-gatherer health and development policy: How the promotion of sedentism worsens the Agta's health outcomes.

Many hunter-gatherer groups live on the outskirts of wider society, experiencing poor health outcomes with little access to medical care. From a development perspective, key interventions include the sedentarisation of these mobile peoples into camps nearby larger towns with sanitation infrastructure and medical care, as increased access to services is assumed to improve outcomes. However, recent research in the Agta (Philippine foragers from North-east Luzon) has demonstrated that individuals residing in more 'developed' communities suffer from increased morbidity and mortality. Here, using quantitative and ethnographic data on health collected between 2002 and 2014, we explore why this trend occurs by examining the relationship between key development initiatives with self-reported illness and the uptake of medical interventions with 415 Agta men, women and children. We demonstrate that health outcomes worsen as sedentarisation progresses, despite some increases in medical access. We argue this is because the development paradigm is not evidence-based, but rather stems from an ideological dislike of mobile hunter-gatherer lifestyles. Compounded by cultural insensitivity and daily discrimination, current interventions are ill-suited to the unique needs of hunter-gatherers, and thus ineffective. Based on our findings we offer future short and long-term policy suggestions which seek to reduce the Agta's vulnerability, rather than increase it.

Cooperation and the evolution of hunter-gatherer storytelling.

Storytelling is a human universal. From gathering around the camp-fire telling tales of ancestors to watching the latest television box-set, humans are inveterate producers and consumers of stories. Despite its ubiquity, little attention has been given to understanding the function and evolution of storytelling. Here we explore the impact of storytelling on hunter-gatherer cooperative behaviour and the individual-level fitness benefits to being a skilled storyteller. Stories told by the Agta, a Filipino hunter-gatherer population, convey messages relevant to coordinating behaviour in a foraging ecology, such as cooperation, sex equality and egalitarianism. These themes are present in narratives from other foraging societies. We also show that the presence of good storytellers is associated with increased cooperation. In return, skilled storytellers are preferred social partners and have greater reproductive success, providing a pathway by which group-beneficial behaviours, such as storytelling, can evolve via individual-level selection. We conclude that one of the adaptive functions of storytelling among hunter gatherers may be to organise cooperation.

Accurate age estimation in small-scale societies.

Precise estimation of age is essential in evolutionary anthropology, especially to infer population age structures and understand the evolution of human life history diversity. However, in small-scale societies, such as hunter-gatherer populations, time is often not referred to in calendar years, and accurate age estimation remains a challenge. We address this issue by proposing a Bayesian approach that accounts for age uncertainty inherent to fieldwork data. We developed a Gibbs sampling Markov chain Monte Carlo algorithm that produces posterior distributions of ages for each individual, based on a ranking order of individuals from youngest to oldest and age ranges for each individual. We first validate our method on 65 Agta foragers from the Philippines with known ages, and show that our method generates age estimations that are superior to previously published regression-based approaches. We then use data on 587 Agta collected during recent fieldwork to demonstrate how multiple partial age ranks coming from multiple camps of hunter-gatherers can be integrated. Finally, we exemplify how the distributions generated by our method can be used to estimate important demographic parameters in small-scale societies: here, age-specific fertility patterns. Our flexible Bayesian approach will be especially useful to improve cross-cultural life history datasets for small-scale societies for which reliable age records are difficult to acquire.

Hunter-Gatherer Social Networks and Reproductive Success.

Individuals' centrality in their social network (who they and their social ties are connected to) has been associated with fertility, longevity, disease and information transmission in a range of taxa. Here, we present the first exploration in humans of the relationship between reproductive success and different measures of network centrality of 39 Agta and 38 BaYaka mothers. We collected three-meter contact ('proximity') networks and reproductive histories to test the prediction that individual centrality is positively associated with reproductive fitness (number of living offspring). Rather than direct social ties influencing reproductive success, mothers with greater indirect centrality (i.e. centrality determined by second and third degree ties) produced significantly more living offspring. However, indirect centrality is also correlated with sickness in the Agta, suggesting a trade-off. In complex social species, the optimisation of individuals' network position has important ramifications for fitness, potentially due to easy access to different parts of the network, facilitating cooperation and social influence in unpredictable ecologies.

Knowledge-Sharing Networks in Hunter-Gatherers and the Evolution of Cumulative Culture.

Humans possess the unique ability for cumulative culture [1, 2]. It has been argued that hunter-gatherer's complex social structure [3-9] has facilitated the evolution of cumulative culture by allowing information exchange among large pools of individuals [10-13]. However, empirical evidence for the interaction between social structure and cultural transmission is scant [14]. Here we examine the reported co-occurrence of plant uses between individuals in dyads (which we define as their "shared knowledge" of plant uses) in BaYaka Pygmies from Congo. We studied reported uses of 33 plants of 219 individuals from four camps. We show that (1) plant uses by BaYaka fall into three main domains: medicinal, foraging, and social norms/beliefs; (2) most medicinal plants have known bioactive properties, and some are positively associated with children's BMI, suggesting that their use is adaptive; (3) knowledge of medicinal plants is mainly shared between spouses and biological and affinal kin; and (4) knowledge of plant uses associated with foraging and social norms is shared more widely among campmates, regardless of relatedness, and is important for camp-wide activities that require cooperation. Our results show the interdependence between social structure and knowledge sharing. We propose that long-term pair bonds, affinal kin recognition, exogamy, and multi-locality create ties between unrelated families, facilitating the transmission of medicinal knowledge and its fitness implications. Additionally, multi-family camps with low inter-relatedness between camp members provide a framework for the exchange of functional information related to cooperative activities beyond the family unit, such as foraging and regulation of social life.