Women's subsistence strategies predict fertility across cultures, but context matters.

While it is commonly assumed that farmers have higher, and foragers lower, fertility compared to populations practicing other forms of subsistence, robust supportive evidence is lacking. We tested whether subsistence activities-incorporating market integration-are associated with fertility in 10,250 women from 27 small-scale societies and found considerable variation in fertility. This variation did not align with group-level subsistence typologies. Societies labeled as "farmers" did not have higher fertility than others, while "foragers" did not have lower fertility. However, at the individual level, we found strong evidence that fertility was positively associated with farming and moderate evidence of a negative relationship between foraging and fertility. Markers of market integration were strongly negatively correlated with fertility. Despite strong cross-cultural evidence, these relationships were not consistent in all populations, highlighting the importance of the socioecological context, which likely influences the diverse mechanisms driving the relationship between fertility and subsistence.

Natural selection of immune and metabolic genes associated with health in two lowland Bolivian populations.

A growing body of work has addressed human adaptations to diverse environments using genomic data, but few studies have connected putatively selected alleles to phenotypes, much less among underrepresented populations such as Amerindians. Studies of natural selection and genotype-phenotype relationships in underrepresented populations hold potential to uncover previously undescribed loci underlying evolutionarily and biomedically relevant traits. Here, we worked with the Tsimane and the Moseten, two Amerindian populations inhabiting the Bolivian lowlands. We focused most intensively on the Tsimane, because long-term anthropological work with this group has shown that they have a high burden of both macro and microparasites, as well as minimal cardiometabolic disease or dementia. We therefore generated genome-wide genotype data for Tsimane individuals to study natural selection, and paired this with blood mRNA-seq as well as cardiometabolic and immune biomarker data generated from a larger sample that included both populations. In the Tsimane, we identified 21 regions that are candidates for selective sweeps, as well as 5 immune traits that show evidence for polygenic selection (e.g., C-reactive protein levels and the response to coronaviruses). Genes overlapping candidate regions were strongly enriched for known involvement in immune-related traits, such as abundance of lymphocytes and eosinophils. Importantly, we were also able to draw on extensive phenotype information for the Tsimane and Moseten and link five regions (containing PSD4, MUC21 and MUC22, TOX2, ANXA6, and ABCA1) with biomarkers of immune and metabolic function. Together, our work highlights the utility of pairing evolutionary analyses with anthropological and biomedical data to gain insight into the genetic basis of health-related traits.

Brain volume, energy balance, and cardiovascular health in two nonindustrial South American populations.

Little is known about brain aging or dementia in nonindustrialized environments that are similar to how humans lived throughout evolutionary history. This paper examines brain volume (BV) in middle and old age among two indigenous South American populations, the Tsimane and Moseten, whose lifestyles and environments diverge from those in high-income nations. With a sample of 1,165 individuals aged 40 to 94, we analyze population differences in cross-sectional rates of decline in BV with age. We also assess the relationships of BV with energy biomarkers and arterial disease and compare them against findings in industrialized contexts. The analyses test three hypotheses derived from an evolutionary model of brain health, which we call the embarrassment of riches (EOR). The model hypothesizes that food energy was positively associated with late life BV in the physically active, food-limited past, but excess body mass and adiposity are now associated with reduced BV in industrialized societies in middle and older ages. We find that the relationship of BV with both non-HDL cholesterol and body mass index is curvilinear, positive from the lowest values to 1.4 to 1.6 SDs above the mean, and negative from that value to the highest values. The more acculturated Moseten exhibit a steeper decrease in BV with age than Tsimane, but still shallower than US and European populations. Lastly, aortic arteriosclerosis is associated with lower BV. Complemented by findings from the United States and Europe, our results are consistent with the EOR model, with implications for interventions to improve brain health.

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.

Adolescence is characterized by more sedentary behaviour and less physical activity even among highly active forager-farmers.

Over 80% of adolescents worldwide are insufficiently active, posing massive public health and economic challenges. Declining physical activity (PA) and sex differences in PA consistently accompany transitions from childhood to adulthood in post-industrialized populations and are attributed to psychosocial and environmental factors. An overarching evolutionary theoretical framework and data from pre-industrialized populations are lacking. This cross-sectional study tests hypotheses from life history theory, that adolescent PA is inversely related to age, but this association is mediated by Tanner stage, reflecting higher and sex-specific energetic demands for growth and reproductive maturation. Detailed measures of PA and pubertal maturation are assessed among Tsimane forager-farmers (age: 7-22 years; 50% female, n = 110). Most Tsimane sampled (71%) meet World Health Organization PA guidelines (greater than or equal to 60 min/day of moderate-to-vigorous PA). Like post-industrialized populations, sex differences and inverse age-activity associations were observed. Tanner stage significantly mediated age-activity associations. Adolescence presents difficulties to PA engagement that warrant further consideration in PA intervention approaches to improve public health.

Paternal provisioning results from ecological change.

Paternal provisioning among humans is puzzling because it is rare among primates and absent in nonhuman apes and because emergent provisioning would have been subject to paternity theft. A provisioning "dad" loses fitness at the hands of nonprovisioning, mate-seeking "cads." Recent models require exacting interplay between male provisioning and female choice to overcome this social dilemma. We instead posit that ecological change favored widespread improvements in male provisioning incentives, and we show theoretically how social obstacles to male provisioning can be overcome. Greater availability of energetically rich, difficult-to-acquire foods enhances female-male and male-male complementarities, thus altering the fitness of dads versus cads. We identify a tipping point where gains from provisioning overcome costs from paternity uncertainty and the dad strategy becomes viable. Stable polymorphic states are possible, meaning that dads need not necessarily eliminate cads. Our simulations suggest that with sufficient complementarities, dads can emerge even in the face of high paternity uncertainty. Our theoretical focus on ecological change as a primary factor affecting the trade-off between male mating and parenting effort suggests different possibilities for using paleo-climatic, archaeological, and genomic evidence to establish the timing of and conditions associated with emergence of paternal provisioning in the hominin lineage.

Matriliny reverses gender disparities in inflammation and hypertension among the Mosuo of China.

Women experience higher morbidity than men, despite living longer. This is often attributed to biological differences between the sexes; however, the majority of societies in which these disparities are observed exhibit gender norms that favor men. We tested the hypothesis that female-biased gender norms ameliorate gender disparities in health by comparing gender differences in inflammation and hypertension among the matrilineal and patrilineal Mosuo of China. Widely reported gender disparities in health were reversed among matrilineal Mosuo compared with patrilineal Mosuo, due to substantial improvements in women's health, with no concomitant detrimental effects on men. These findings offer evidence that gender norms limiting women's autonomy and biasing inheritance toward men adversely affect the health of women, increasing women's risk for chronic diseases with tremendous global health impact.

Prevalence of dementia and mild cognitive impairment in indigenous Bolivian forager-horticulturalists.

INTRODUCTION: We evaluated the prevalence of dementia and mild cognitive impairment (MCI) in indigenous Tsimane and Moseten, who lead a subsistence lifestyle. METHODS: Participants from population-based samples ≥ 60 years of age (n = 623) were assessed using adapted versions of the Modified Mini-Mental State Examination, informant interview, longitudinal cognitive testing and brain computed tomography (CT) scans. RESULTS: Tsimane exhibited five cases of dementia (among n = 435; crude prevalence = 1.2%, 95% confidence interval [CI]: 0.4, 2.7); Moseten exhibited one case (among n = 169; crude prevalence = 0.6%, 95% CI: 0.0, 3.2), all age ≥ 80 years. Age-standardized MCI prevalence was 7.7% (95% CI: 5.2, 10.3) in Tsimane and 9.8% (95% CI: 4.9, 14.6) in Moseten. Cognitive impairment was associated with visuospatial impairments, parkinsonian symptoms, and vascular calcification in the basal ganglia. DISCUSSION: The prevalence of dementia in this cohort is among the lowest in the world. Widespread intracranial medial arterial calcifications suggest a previously unrecognized, non-Alzheimer's disease (AD) dementia phenotype.

The multinomial index: a robust measure of reproductive skew.

Inequality or skew in reproductive success (RS) is common across many animal species and is of long-standing interest to the study of social evolution. However, the measurement of inequality in RS in natural populations has been challenging because existing quantitative measures are highly sensitive to variation in group/sample size, mean RS, and age-structure. This makes comparisons across multiple groups and/or species vulnerable to statistical artefacts and hinders empirical and theoretical progress. Here, we present a new measure of reproductive skew, the multinomial index, M, that is unaffected by many of the structural biases affecting existing indices. M is analytically related to Nonacs' binomial index, B, and comparably accounts for heterogeneity in age across individuals; in addition, M allows for the possibility of diminishing or even highly nonlinear RS returns to age. Unlike B, however, M is not biased by differences in sample/group size. To demonstrate the value of our index for cross-population comparisons, we conduct a reanalysis of male reproductive skew in 31 primate species. We show that a previously reported negative effect of group size on mating skew was an artefact of structural biases in existing skew measures, which inevitably decline with group size; this bias disappears when using M. Applying phylogenetically controlled, mixed-effects models to the same dataset, we identify key similarities and differences in the inferred within- and between-species predictors of reproductive skew across metrics. Finally, we provide an R package, SkewCalc, to estimate M from empirical data.

Inclusive fitness and differential productivity across the life course determine intergenerational transfers in a small-scale human society.

Transfers of resources between generations are an essential element in current models of human life-history evolution accounting for prolonged development, extended lifespan and menopause. Integrating these models with Hamilton's theory of inclusive fitness, we predict that the interaction of biological kinship with the age-schedule of resource production should be a key driver of intergenerational transfers. In the empirical case of Tsimane' forager-horticulturalists in Bolivian Amazonia, we provide a detailed characterization of net transfers of food according to age, sex, kinship and the net need of donors and recipients. We show that parents, grandparents and siblings provide significant net downward transfers of food across generations. We demonstrate that the extent of provisioning responds facultatively to variation in the productivity and demographic composition of families, as predicted by the theory. We hypothesize that the motivation to provide these critical transfers is a fundamental force that binds together human nuclear and extended families. The ubiquity of three-generational families in human societies may thus be a direct reflection of fundamental evolutionary constraints on an organism's life-history and social organization.

Skill ontogeny among Tsimane forager-horticulturalists.

OBJECTIVES: We investigate whether age profiles of Tsimane forager-horticulturalists' reported skill development are consistent with predictions derived from life history theory about the timing of productivity and reproduction. Previous studies of forager skill development have often focused on a few abilities (e.g. hunting), and neglected the broad range of skills and services typical of forager economies (e.g. childcare, craft production, music performance, story-telling). MATERIALS AND METHODS: By systematically examining age patterns in reported acquisition, proficiency, and expertise across a broad range of activities including food production, childcare, and other services, we provide the most complete skill development study of a traditional subsistence society to date. RESULTS: Our results show that: (1) most essential skills are acquired prior to first reproduction, then developed further so that their productive returns meet the increasing demands of dependent offspring during adulthood; (2) as postreproductive adults age beyond earlier years of peak performance, they report developing additional conceptual and procedural proficiency, and despite greater physical frailty than younger adults, are consensually regarded as the most expert (especially in music and storytelling), consistent with their roles as providers and educators. We find that adults have accurate understandings of their skillsets and skill levels -an important awareness for social exchange, comparison, learning, and pedagogy. DISCUSSION: These findings extend our understanding of the evolved human life history by illustrating how changes in embodied capital and the needs of dependent offspring predict the development of complementary skills and services in a forager-horticulturalist economy.

Cross-cousin marriage among Tsimane forager-horticulturalists during demographic transition and market integration.

Although still prevalent in many human societies, the practice of cousin marriage has precipitously declined in populations undergoing rapid demographic and socioeconomic change. However, it is still unclear whether changes in the structure of the marriage pool or changes in the fitness-relevant consequences of cousin marriage more strongly influence the frequency of cousin marriage. Here, we use genealogical data collected by the Tsimane Health and Life History Project to show that there is a small but measurable decline in the frequency of first cross-cousin marriage since the mid-twentieth century. Such changes are linked to concomitant changes in the pool of potential spouses in recent decades. We find only very modest differences in fitness-relevant demographic measures between first cousin and non-cousin marriages. These differences have been diminishing as the Tsimane have become more market integrated. The factors that influence preferences for cousin marriage appear to be less prevalent now than in the past, but cultural inertia might slow the pace of change in marriage norms. Overall, our findings suggest that cultural changes in marriage practices reflect underlying societal changes that shape the pool of potential spouses.

Poor Oral Health Is Associated With Inflammation, Aortic Valve Calcification, and Brain Volume Among Forager-Farmers.

Poor oral health is associated with cardiovascular disease and dementia. Potential pathways include sepsis from oral bacteria, systemic inflammation, and nutritional deficiencies. However, in post-industrialized populations, links between oral health and chronic disease may be confounded because the lower socioeconomic exposome (poor diet, pollution, and low physical activity) often entails insufficient dental care. We assessed tooth loss, caries, and damaged teeth, in relation to cardiovascular and brain aging among the Tsimane, a subsistence population living a relatively traditional forager-horticulturalist lifestyle with poor dental health, but minimal cardiovascular disease and dementia. Dental health was assessed by a physician in 739 participants aged 40-92 years with cardiac and brain health measured by chest computed tomography (CT; n = 728) and brain CT (n = 605). A subset of 356 individuals aged 60+ were also assessed for dementia and mild cognitive impairment (n = 33 impaired). Tooth loss was highly prevalent, with 2.2 teeth lost per decade and a 2-fold greater loss in women. The number of teeth with exposed pulp was associated with higher inflammation, as measured by cytokine levels and white blood cell counts, and lower body mass index. Coronary artery calcium and thoracic aortic calcium were not associated with tooth loss or damaged teeth. However, aortic valve calcification and brain tissue loss were higher in those who had more teeth with exposed pulp. Overall, these results suggest that dental health is associated with indicators of chronic diseases in the absence of typical confounds, even in a population with low cardiovascular and dementia risk factors.

Increases in regional brain volume across two native South American male populations.

Industrialized environments, despite benefits such as higher levels of formal education and lower rates of infections, can also have pernicious impacts upon brain atrophy. Partly for this reason, comparing age-related brain volume trajectories between industrialized and non-industrialized populations can help to suggest lifestyle correlates of brain health. The Tsimane, indigenous to the Bolivian Amazon, derive their subsistence from foraging and horticulture and are physically active. The Moseten, a mixed-ethnicity farming population, are physically active but less than the Tsimane. Within both populations (N = 1024; age range = 46-83), we calculated regional brain volumes from computed tomography and compared their cross-sectional trends with age to those of UK Biobank (UKBB) participants (N = 19,973; same age range). Surprisingly among Tsimane and Moseten (T/M) males, some parietal and occipital structures mediating visuospatial abilities exhibit small but significant increases in regional volume with age. UKBB males exhibit a steeper negative trend of regional volume with age in frontal and temporal structures compared to T/M males. However, T/M females exhibit significantly steeper rates of brain volume decrease with age compared to UKBB females, particularly for some cerebro-cortical structures (e.g., left subparietal cortex). Across the three populations, observed trends exhibit no interhemispheric asymmetry. In conclusion, the age-related rate of regional brain volume change may differ by lifestyle and sex. The lack of brain volume reduction with age is not known to exist in other human population, highlighting the putative role of lifestyle in constraining regional brain atrophy and promoting elements of non-industrialized lifestyle like higher physical activity.

Dynamical Structure of a Traditional Amazonian Social Network.

Reciprocity is a vital feature of social networks, but relatively little is known about its temporal structure or the mechanisms underlying its persistence in real world behavior. In pursuit of these two questions, we study the stationary and dynamical signals of reciprocity in a network of manioc beer (Spanish: chicha; Tsimane': shocdye') drinking events in a Tsimane' village in lowland Bolivia. At the stationary level, our analysis reveals that social exchange within the community is heterogeneously patterned according to kinship and spatial proximity. A positive relationship between the frequencies at which two families host each other, controlling for kinship and proximity, provides evidence for stationary reciprocity. Our analysis of the dynamical structure of this network presents a novel method for the study of conditional, or non-stationary, reciprocity effects. We find evidence that short-timescale reciprocity (within three days) is present among non- and distant-kin pairs; conversely, we find that levels of cooperation among close kin can be accounted for on the stationary hypothesis alone.

Adolescence is characterized by more sedentary behavior and less physical activity even among highly active forager-farmers.

Over 80% of adolescents worldwide are insufficiently active, posing massive public health and economic challenges. Declining physical activity (PA) and sex differences in PA consistently accompany transitions from childhood to adulthood in post-industrialized populations and are attributed to psychosocial and environmental factors. An overarching evolutionary theoretical framework and data from pre-industrialized populations are lacking. In this cross-sectional study we test a hypothesis from life history theory, that adolescent PA reductions reflect an evolved strategy to conserve energy, given the increasing sex-specific energetic demands for growth and reproductive maturation. Detailed measures of PA and pubertal maturation are assessed among Tsimane forager-farmers (age: 7-22 yrs.; 50% female, n=110). We find that 71% of Tsimane sampled meet World Health Organization PA guidelines (≥60 minutes/day of moderate-to-vigorous PA). Consistent with post-industrialized populations, we observe sex differences and inverse age-activity associations mediated by Tanner stage. Physical inactivity in adolescence is distinct from other health risk behaviors and also not merely resulting from obesogenic environments.

Inheritance and inequality among nomads of South Siberia.

At the headwaters of the Yenisei River in Tuva and northern Mongolia, nomadic pastoralists move between camps in a seasonal rotation that facilitates their animals' access to high-quality grasses and shelter. The use and informal ownership of these camps depending on season helps illustrate evolutionary and ecological principles underlying variation in property relations. Given relatively stable patterns of precipitation and returns to capital improvement, families generally benefit from reusing the same camps year after year. We show that locations with higher economic defensibility and capital investment-winter camps and camps located in mountain/river valleys-are claimed and inherited more frequently than summer camps and camps located in open steppe. Camps are inherited patrilineally and matrilineally at a ratio of 2 : 1. Despite its practical importance, camp inheritance is not associated with livestock wealth today, which is better predicted by education and wealth outside the pastoral economy. The relationship between the livestock wealth of parents and their adult children is significantly positive, but relatively low compared to other pastoralists. The degree of inequality in livestock wealth, however, is very close to that of other pastoralists. This is understandable considering the durability and defensibility of animal wealth and economies of scale common across pastoralists. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Gains to cooperation drive the evolution of egalitarianism.

What conditions favour egalitarianism, that is, muted hierarchies with relatively equal distributions of resources? Here, we combine the hawk-dove and prisoner's dilemma games to model the effects of economic defensibility, costs of competition and gains from cooperation on egalitarianism, operationalized as the absence of hawks. We show that a 'leveller' strategy, which punishes hawkishness in the hawk-dove game with defection in the prisoner's dilemma, can be evolutionarily stable provided that the gains from cooperation are high relative to the benefits of hawkishness. Under these conditions, rare mutant levellers select for hawks that acquiesce to punishment by playing dove. If these 'acquiescent hawks' become common, levellers outperform hawks and establish a new egalitarian equilibrium. An analysis of human foraging groups corroborates these results, as groups with a greater reliance on cooperation are more egalitarian. Cooperation fosters greater equality when individuals can withhold its benefits from would-be dominant individuals.

Do wealth and inequality associate with health in a small-scale subsistence society?

In high-income countries, one's relative socio-economic position and economic inequality may affect health and well-being, arguably via psychosocial stress. We tested this in a small-scale subsistence society, the Tsimane, by associating relative household wealth (n = 871) and community-level wealth inequality (n = 40, Gini = 0.15-0.53) with a range of psychological variables, stressors, and health outcomes (depressive symptoms [n = 670], social conflicts [n = 401], non-social problems [n = 398], social support [n = 399], cortisol [n = 811], body mass index [n = 9,926], blood pressure [n = 3,195], self-rated health [n = 2523], morbidities [n = 1542]) controlling for community-average wealth, age, sex, household size, community size, and distance to markets. Wealthier people largely had better outcomes while inequality associated with more respiratory disease, a leading cause of mortality. Greater inequality and lower wealth were associated with higher blood pressure. Psychosocial factors did not mediate wealth-health associations. Thus, relative socio-economic position and inequality may affect health across diverse societies, though this is likely exacerbated in high-income countries.

Poverty is bad for health. People living in poverty are more likely to struggle to afford nutritious food, lack access to health care, or be overworked or stressed. This may make them susceptible to chronic diseases, contribute to faster aging, and shorten their lifespans. In high-income countries, there is growing evidence to suggest that a person's 'rank' in society also impacts their health. For example, individuals who have a lower position in the social hierarchy report worse health outcomes, regardless of their incomes. But it is unclear why living in an unequal society or having a lower social status contributes to poorer health. One possibility is that inequalities in society are creating a stressful environment that leads to worse physical and mental outcomes. It is thought that this stress largely comes from how humans evolved to prioritize reaching a higher social status over having a long and healthy life. If this is the case, this would mean that the link between social status and health would also be present in non-industrialized communities where social hierarchies tend to be less pronounced. To test this, Jaeggi, Blackwell et al. studied the Indigenous Tsimane population in Bolivia who live in small communities and forage and farm their own food. The income and relative wealth of 870 households from 40 Tsimane communities were compared against various outcomes, including symptoms associated with depression, stress hormone levels, blood pressure, self-rated health and several diseases. Jaeggi, Blackwell et al. found poverty and inequality did not negatively impact all of the health outcomes measured as has been previously reported for industrialized societies. However, blood pressure was higher among people with lower incomes or those who lived in more unequal communities. But because the Tsimane people generally have low blood pressure, the differences were too small to have much effect on their health. People who lived in more unequal communities were also three times more likely to have respiratory infections, but the reason for this was unclear. This shows that social determinants such as a person's wealth or inequality can affect health, even in communities with less rigid social hierarchies. In industrial societies the effect may be worse in part because they are compounded by lifestyle factors, such as diets rich in fat and sugar, and physical inactivity which can also increase blood pressure. This information may help policy makers reduce health disparities by addressing some of the social determinants of health and the lifestyle factors that cause them.

The Indigenous South American Tsimane Exhibit Relatively Modest Decrease in Brain Volume With Age Despite High Systemic Inflammation.

Brain atrophy is correlated with risk of cognitive impairment, functional decline, and dementia. Despite a high infectious disease burden, Tsimane forager-horticulturists of Bolivia have the lowest prevalence of coronary atherosclerosis of any studied population and present few cardiovascular disease (CVD) risk factors despite a high burden of infections and therefore inflammation. This study (a) examines the statistical association between brain volume (BV) and age for Tsimane and (b) compares this association to that of 3 industrialized populations in the United States and Europe. This cohort-based panel study enrolled 746 participants aged 40-94 (396 males), from whom computed tomography (CT) head scans were acquired. BV and intracranial volume (ICV) were calculated from automatic head CT segmentations. The linear regression coefficient estimate ß^T of the Tsimane (T), describing the relationship between age (predictor) and BV (response, as a percentage of ICV), was calculated for the pooled sample (including both sexes) and for each sex. ß^T was compared to the corresponding regression coefficient estimate ß^R of samples from the industrialized reference (R) countries. For all comparisons, the null hypothesis ß T = ß R was rejected both for the combined samples of males and females, as well as separately for each sex. Our results indicate that the Tsimane exhibit a significantly slower decrease in BV with age than populations in the United States and Europe. Such reduced rates of BV decrease, together with a subsistence lifestyle and low CVD risk, may protect brain health despite considerable chronic inflammation related to infectious burden.