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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.
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Reproducción , Caracteres Sexuales , Animales , Humanos , Femenino , Masculino , Matrimonio , Mamíferos , Conducta Sexual AnimalRESUMEN
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.
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Polimorfismo Genético , Receptores Sensibles al Calcio , Animales , Humanos , Ratones , Calcio , Fenotipo , Receptores Sensibles al Calcio/genética , Selección GenéticaRESUMEN
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.
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Antropología Cultural , Arqueología , Variación Genética , Densidad de Población , África , Agricultura , Diversidad Cultural , HumanosRESUMEN
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.
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Envejecimiento , Antropología/métodos , Adolescente , Adulto , Distribución por Edad , Anciano , Anciano de 80 o más Años , Teorema de Bayes , Femenino , Fertilidad , Humanos , Cadenas de Markov , Persona de Mediana Edad , Filipinas , Densidad de Población , Reproducibilidad de los Resultados , Sociedades , IncertidumbreRESUMEN
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.
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The Neolithic demographic transition remains a paradox, because it is associated with both higher rates of population growth and increased morbidity and mortality rates. Here we reconcile the conflicting evidence by proposing that the spread of agriculture involved a life history quality-quantity trade-off whereby mothers traded offspring survival for increased fertility, achieving greater reproductive success despite deteriorating health. We test this hypothesis by investigating fertility, mortality, health, and overall reproductive success in Agta hunter-gatherers whose camps exhibit variable levels of sedentarization, mobility, and involvement in agricultural activities. We conducted blood composition tests in 345 Agta and found that viral and helminthic infections as well as child mortality rates were significantly increased with sedentarization. Nonetheless, both age-controlled fertility and overall reproductive success were positively affected by sedentarization and participation in cultivation. Thus, we provide the first empirical evidence, to our knowledge, of an adaptive mechanism in foragers that reconciles the decline in health and child survival with the observed demographic expansion during the Neolithic.
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Adaptación Fisiológica/fisiología , Dieta Paleolítica/estadística & datos numéricos , Modelos Biológicos , Crecimiento Demográfico , Reproducción/fisiología , Arqueología/métodos , Simulación por Computador , Humanos , Modelos Estadísticos , FilipinasRESUMEN
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.
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Crianza del Niño/etnología , Relaciones Familiares/etnología , Adulto , Preescolar , Congo/etnología , Femenino , Humanos , Lactante , Masculino , Malí/etnología , Filipinas/etnologíaRESUMEN
Human evolutionary history in Central Africa reflects a deep history of population connectivity. However, Central African hunter-gatherers (CAHGs) currently speak languages acquired from their neighbouring farmers. Hence it remains unclear which aspects of CAHG cultural diversity results from long-term evolution preceding agriculture and which reflect borrowing from farmers. On the basis of musical instruments, foraging tools, specialized vocabulary and genome-wide data from ten CAHG populations, we reveal evidence of large-scale cultural interconnectivity among CAHGs before and after the Bantu expansion. We also show that the distribution of hunter-gatherer musical instruments correlates with the oldest genomic segments in our sample predating farming. Music-related words are widely shared between western and eastern groups and likely precede the borrowing of Bantu languages. In contrast, subsistence tools are less frequently exchanged and may result from adaptation to local ecologies. We conclude that CAHG material culture and specialized lexicon reflect a long evolutionary history in Central Africa.
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Evolución Cultural , Lenguaje , Lingüística , Humanos , África Central , Música , Agricultura/historia , Población NegraRESUMEN
Human pygmy populations inhabit different regions of the world, from Africa to Melanesia. In Asia, short-statured populations are often referred to as "negritos." Their short stature has been interpreted as a consequence of thermoregulatory, nutritional, and/or locomotory adaptations to life in tropical forests. A more recent hypothesis proposes that their stature is the outcome of a life history trade-off in high-mortality environments, where early reproduction is favored and, consequently, early sexual maturation and early growth cessation have coevolved. Some serological evidence of deficiencies in the growth hormone/insulin-like growth factor axis have been previously associated with pygmies' short stature. Using genome-wide single-nucleotide polymorphism genotype data, we first tested whether different negrito groups living in the Philippines and Papua New Guinea are closely related and then investigated genomic signals of recent positive selection in African, Asian, and Papuan pygmy populations. We found that negritos in the Philippines and Papua New Guinea are genetically more similar to their nonpygmy neighbors than to one another and have experienced positive selection at different genes. These results indicate that geographically distant pygmy groups are likely to have evolved their short stature independently. We also found that selection on common height variants is unlikely to explain their short stature and that different genes associated with growth, thyroid function, and sexual development are under selection in different pygmy groups.
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Adaptación Fisiológica/genética , Pueblo Asiatico/genética , Evolución Biológica , Población Negra/genética , Estatura/genética , Genética de Población , Nativos de Hawái y Otras Islas del Pacífico/genética , Antropología Física , Pueblo Asiatico/etnología , Población Negra/etnología , Estatura/etnología , Variación Genética , Genotipo , Humanos , Nativos de Hawái y Otras Islas del Pacífico/etnología , Papúa Nueva Guinea/etnología , Fenotipo , Filipinas/etnología , Polimorfismo de Nucleótido SimpleRESUMEN
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.
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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'.
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Evolución Cultural , Hominidae , Animales , Arqueología , Evolución Biológica , Humanos , Inteligencia , Conducta SocialRESUMEN
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.
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Evolución Cultural , Antropología Cultural , ArqueologíaRESUMEN
Anthropologists have long been fascinated by the isolated hunter-gatherer populations in Southeast Asia (SEA) collectively known as "Negritos." However, the origins and affinities of these groups remain unresolved. Negritos are characterized by their short stature, dark skin color, and wiry hair, and they inhabit the Philippines, Malay Peninsula, and the Andaman Islands. Among Philippine Negritos, the Batak are of particular interest in understanding population interactions in the region due to their location on Palawan Island, which likely formed a corridor by which human migrations entered the rest of the Philippine archipelago from Island SEA. Here, we extend current understanding of the distribution of genetic diversity in Negritos by presenting the first analysis of mitochondrial DNA and Y-chromosome diversity among the Batak. We show that the Batak are genetically distinct from Negritos of the Andaman Islands and Malay Peninsula and instead bear most resemblance to geographically proximate Philippine Negritos and to non-Negrito populations from the Philippines and Island SEA. An extensive degree of recent admixture between the Batak and their neighbors is indicated by the high frequency of recently coalescing haplogroups in the Batak that are found throughout Island SEA. The comparison of results from these two loci further lends support to the hypothesis that male-biased admixture has, in particular, been a prominent feature of the interactions between the Batak and surrounding non-Negrito populations.
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Pueblo Asiatico/genética , Variación Genética , Filogenia , Análisis de Varianza , Cromosomas Humanos Y , ADN Mitocondrial/genética , Genética de Población , Haplotipos , Humanos , Masculino , Filipinas , Dinámica PoblacionalRESUMEN
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.
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Explanations for the evolution of human pygmies continue to be a matter of controversy, recently fuelled by the disagreements surrounding the interpretation of the fossil hominin Homo floresiensis. Traditional hypotheses assume that the small body size of human pygmies is an adaptation to special challenges, such as thermoregulation, locomotion in dense forests, or endurance against starvation. Here, we present an analysis of stature, growth, and individual fitness for a large population of Aeta and a smaller one of Batak from the Philippines and compare it with data on other pygmy groups accumulated by anthropologists for a century. The results challenge traditional explanations of human pygmy body size. We argue that human pygmy populations and adaptations evolved independently as the result of a life history tradeoff between the fertility benefits of larger body size against the costs of late growth cessation, under circumstances of significant young and adult mortality. Human pygmies do not appear to have evolved through positive selection for small stature-this was a by-product of selection for early onset of reproduction.
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Evolución Biológica , Fósiles , Fertilidad , Historia Antigua , Humanos , Vida , Mortalidad , FilipinasRESUMEN
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.
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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.
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Mamíferos , Conducta Social , Animales , Evolución BiológicaRESUMEN
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.
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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.
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Aprendizaje/fisiología , Aprendizaje Social/fisiología , Niño , Congo , Conducta Cooperativa , Evolución Cultural , Femenino , Humanos , Conocimiento , Masculino , Caracteres Sexuales , Conducta SocialRESUMEN
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.