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.

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.

Voluntary collective isolation as a best response to COVID-19 for indigenous populations? A case study and protocol from the Bolivian Amazon.

Indigenous communities worldwide share common features that make them especially vulnerable to the complications of and mortality from COVID-19. They also possess resilient attributes that can be leveraged to promote prevention efforts. How can indigenous communities best mitigate potential devastating effects of COVID-19? In Bolivia, where nearly half of all citizens claim indigenous origins, no specific guidelines have been outlined for indigenous communities inhabiting native communal territories. In this Public Health article, we describe collaborative efforts, as anthropologists, physicians, tribal leaders, and local officials, to develop and implement a multiphase COVID-19 prevention and containment plan focused on voluntary collective isolation and contact-tracing among Tsimane forager-horticulturalists in the Bolivian Amazon. Phase 1 involves education, outreach, and preparation, and phase 2 focuses on containment, patient management, and quarantine. Features of this plan might be exported and adapted to local circumstances elsewhere to prevent widespread mortality in indigenous communities.

Information transmission and the oral tradition: Evidence of a late-life service niche for Tsimane Amerindians.

Storytelling can affect wellbeing and fitness by transmitting information and reinforcing cultural codes of conduct. Despite their potential importance, the development and timing of storytelling skills, and the transmission of story knowledge have received minimal attention in studies of subsistence societies that more often focus on food production skills. Here we examine how storytelling and patterns of information transmission among Tsimane forager-horticulturalists are predicted by the changing age profiles of storytellers' abilities and accumulated experience. We find that storytelling skills are most developed among older adults who demonstrate superior knowledge of traditional stories and who report telling stories most. We find that the important information transmitted via storytelling typically flows from older to younger generations, and stories are primarily learned from older same-sex relatives, especially grandparents. Our findings suggest that the oral tradition provides a specialized late-life service niche for Tsimane adults who have accumulated important experience and knowledge relevant to foraging and sociality, but have lost comparative advantage in other productive domains. These findings may help extend our understanding of the evolved human life history by illustrating how changes in embodied capital predict the development of information transmission services in a forager-horticulturalist economy.

High resting metabolic rate among Amazonian forager-horticulturalists experiencing high pathogen burden.

OBJECTIVES: Resting metabolic rate (RMR) reflects energetic costs of homeostasis and accounts for 60 to 75% of total energy expenditure (TEE). Lean mass and physical activity account for much RMR variability, but the impact of prolonged immune activation from infection on human RMR is unclear in naturalistic settings. We evaluate the effects of infection on mass-corrected RMR among Bolivian forager-horticulturalists, and assess whether RMR declines more slowly with age than in hygienic sedentary populations, as might be expected if older adults experience high pathogen burden. MATERIALS AND METHODS: RMR was measured by indirect calorimetry (Fitmate MED, Cosmed) in 1,300 adults aged 20 to 90 and TEE was measured using doubly labeled water (n = 40). Immune biomarkers, clinical diagnoses, and anthropometrics were collected by the Tsimane Health and Life History Project. RESULTS: Tsimane have higher RMR and TEE than people in sedentary industrialized populations. Tsimane RMR is 18 to 47% (women) and 22 to 40% (men) higher than expected using six standard prediction equations. Tsimane mass-corrected TEE is similarly elevated compared to Westerners. Elevated leukocytes and helminths are associated with excess RMR in multivariate regressions, and jointly result in a predicted excess RMR of 10 to 15%. After age 40, RMR declines by 69 kcal/decade (p < .0001). Controlling for lean mass and height accounts for 71% of age-related RMR decline, and adding indicators of infection minimally affects the age slope. The residual level of age-related decline from age 40 is 1.2% per decade. CONCLUSION: High pathogen burden may lead to higher metabolic costs, which may be offset by smaller body mass or other energy-sparing mechanisms.

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.

Salivary oxytocin increases concurrently with testosterone and time away from home among returning Tsimane' hunters.

Oxytocin, testosterone and cortisol can have opposing effects on social behaviour, yet few studies have examined their interactions. We measured changes in salivary oxytocin, testosterone and cortisol among Tsimane' men returning home after hunting, an ancient context of male status competition, parental investment and cooperation. Contra normal diurnal rhythm, oxytocin increased relative to baseline and this increase was positively associated with duration of the hunt and change in testosterone, but not cortisol, social context, hunting outcome or physical activity. The concurrent increase in endogenous peripheral oxytocin and testosterone is unexpected given their opposing independent effects on social cognition and behaviour, and has not been observed before. We discuss the potential significance of these effects for the biology of pair-bonding, parenting and social foraging in humans and other species.

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.

Successful hunting increases testosterone and cortisol in a subsistence population.

Controversy over the adaptive significance of male hunting in subsistence societies hinges on the relative importance of familial provisioning and mate-quality signalling. This paper examines the proximate and ultimate motivations of hunting behaviour from a neuroendocrine perspective, using salivary testosterone and cortisol data collected before, during and after hunting focal follows from 31 Tsimane hunters aged 18-82 years. Despite circadian declines in hormone levels, testosterone and cortisol of Tsimane hunters increased at the time of a kill, and remained high as successful hunters returned home. Previous studies of hormonal changes during competitions find that high-stakes and success in the presence of relevant audiences result in increased neuroendocrine arousal. If men hunt primarily to provision their families, then an additional audience would not be expected to impact testosterone or cortisol, nor would the size of the animal killed. However, if signalling male quality by 'showing off' was a larger relative driver of men's hunting behaviour, one would expect greater hormonal response in cases where men returned with large sharable kills, especially in the presence of community members. Consistent with provisioning models of male hunting motivation, neither kill size nor encountering an audience of villagers while returning from hunting was associated with hormonal changes for successful hunters.

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.

Age-independent increases in male salivary testosterone during horticultural activity among Tsimane forager-farmers.

Testosterone plays an important role in mediating male reproductive trade-offs in many vertebrate species, augmenting muscle and influencing behavior necessary for male-male competition and mating-effort. Among humans, testosterone may also play a key role in facilitating male provisioning of offspring as muscular and neuromuscular performance are deeply influenced by acute changes in testosterone. This study examines acute changes in salivary testosterone among 63 Tsimane men ranging in age from 16-80 (mean 38.2) years during one-hour bouts of tree-chopping while clearing horticultural plots. The Tsimane forager-horticulturalists living in the Bolivian Amazon experience high energy expenditure associated with food production, have high levels of parasites and pathogens, and display significantly lower baseline salivary testosterone than age-matched US males. Mixed-effects models controlling for BMI and time of specimen collection reveal increased salivary testosterone (p<0.001) equivalent to a 48.6% rise, after one hour of tree chopping. Age had no effect on baseline (p=0.656) or change in testosterone (p=0.530); self-reported illness did not modify testosterone change (p=0.488). A comparison of these results to the relative change in testosterone during a competitive soccer tournament in the same population reveals larger relative changes in testosterone following resource production (tree chopping), compared to competition (soccer). These findings highlight the importance of moving beyond a unidimensional focus on changes in testosterone and male-male aggression to investigate the importance of testosterone-behavior interactions across additional male fitness-related activities. Acutely increased testosterone during muscularly intensive horticultural food production may facilitate male productivity and provisioning.

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.

Risk and the evolution of human exchange.

Compared with other species, exchange among non-kin is a hallmark of human sociality in both the breadth of individuals and total resources involved. One hypothesis is that extensive exchange evolved to buffer the risks associated with hominid dietary specialization on calorie dense, large packages, especially from hunting. 'Lucky' individuals share food with 'unlucky' individuals with the expectation of reciprocity when roles are reversed. Cross-cultural data provide prima facie evidence of pair-wise reciprocity and an almost universal association of high-variance (HV) resources with greater exchange. However, such evidence is not definitive; an alternative hypothesis is that food sharing is really 'tolerated theft', in which individuals possessing more food allow others to steal from them, owing to the threat of violence from hungry individuals. Pair-wise correlations may reflect proximity providing greater opportunities for mutual theft of food. We report a laboratory experiment of foraging and food consumption in a virtual world, designed to test the risk-reduction hypothesis by determining whether people form reciprocal relationships in response to variance of resource acquisition, even when there is no external enforcement of any transfer agreements that might emerge. Individuals can forage in a high-mean, HV patch or a low-mean, low-variance (LV) patch. The key feature of the experimental design is that individuals can transfer resources to others. We find that sharing hardly occurs after LV foraging, but among HV foragers sharing increases dramatically over time. The results provide strong support for the hypothesis that people are pre-disposed to evaluate gains from exchange and respond to unsynchronized variance in resource availability through endogenous reciprocal trading relationships.

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

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

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.

Very Low Prevalence and Incidence of Atrial Fibrillation among Bolivian Forager-Farmers.

Background: Atrial fibrillation is the most common arrhythmia in post-industrialized populations. Older age, hypertension, obesity, chronic inflammation, and diabetes are significant atrial fibrillation risk factors, suggesting that modern urban environments may promote atrial fibrillation. Objective: Here we assess atrial fibrillation prevalence and incidence among tropical horticulturalists of the Bolivian Amazon with high levels of physical activity, a lean diet, and minimal coronary atherosclerosis, but also high infectious disease burden and associated inflammation. Methods: Between 2005-2019, 1314 Tsimane aged 40-94 years (52% female) and 534 Moseten Amerindians aged 40-89 years (50% female) underwent resting 12-lead electrocardiograms to assess atrial fibrillation prevalence. For atrial fibrillation incidence assessment, 1059 (81% of original sample) Tsimane and 310 Moseten (58%) underwent additional ECGs (mean time to follow up 7.0, 1.8 years, respectively). Findings: Only one (male) of 1314 Tsimane (0.076%) and one (male) of 534 Moseten (0.187%) demonstrated atrial fibrillation at baseline. There was one new (female) Tsimane case in 7395 risk years for the 1059 participants with >1 ECG (incidence rate = 0.14 per 1,000 risk years). No new cases were detected among Moseten, based on 542 risk years. Conclusion: Tsimane and Moseten show the lowest levels of atrial fibrillation ever reported, 1/20 to ~1/6 of rates in high-income countries. These findings provide additional evidence that a subsistence lifestyle with high levels of physical activity, and a diet low in processed carbohydrates and fat is cardioprotective, despite frequent infection-induced inflammation. Findings suggest that atrial fibrillation is a modifiable lifestyle disease rather than an inevitable feature of cardiovascular aging.

A theory of leadership in human cooperative groups.

Two types of models aim to account the origins of rank differentiation and social hierarchy in human societies. Conflict models suggest that the formation of social hierarchies is synonymous with the establishment of relationships of coercive social dominance and exploitation. Voluntary or 'integrative' models, on the other hand, suggest that rank differentiation--the differentiation of leader from follower, ruler from ruled, or state from subject--may sometimes be preferred over more egalitarian social arrangements as a solution to the challenges of life in social groups, such as conflict over resources, coordination failures, and free-riding in cooperative relationships. Little formal theoretical work, however, has established whether and under what conditions individuals would indeed prefer the establishment of more hierarchical relationships over more egalitarian alternatives. This paper provides an evolutionary game theoretical model for the acceptance of leadership in cooperative groups. We propose that the effort of a leader can reduce the likelihood that cooperation fails due to free-riding or coordination errors, and that under some circumstances, individuals would prefer to cooperate in a group under the supervision of a leader who receives a share of the group's productivity than to work in an unsupervised group. We suggest, in particular, that this becomes an optimal solution for individual decision makers when the number of group members required for collective action exceeds the maximum group size at which leaderless cooperation is viable.

We age because we grow.

Why do we age? Since ageing is a near-universal feature of complex organisms, a convincing theory must provide a robust evolutionary explanation for its ubiquity. This theory should be compatible with the physiological evidence that ageing is largely due to deterioration, which is, in principle, reversible through repair. Moreover, this theory should also explain why natural selection has favoured organisms that first improve with age (mortality rates decrease) and then deteriorate with age (mortality rates rise). We present a candidate for such a theory of life history, applied initially to a species with determinate growth. The model features both the quantity and the quality of somatic capital, where it is optimal to initially build up quantity, but to allow quality to deteriorate. The main theoretical result of the paper is that a life history where mortality decreases early in life and then increases late in life is evolutionarily optimal. In order to apply the model to humans, in particular, we include a budget constraint to allow intergenerational transfers. The resultant theory then accounts for all our basic demographic characteristics, including menopause with extended survival after reproduction has ceased.

Experimental tests of the tolerated theft and risk-reduction theories of resource exchange.

Here we report the results of an experiment that tests the reciprocal risk reduction 1 and 'tolerated theft' or taking hypotheses 2 for why the human species is unique in having extensive exchange of resources among non-kin. We designed an experiment to determine whether, in response to variance of resource acquisition, people exchange food resources via taking or, alternatively, form reciprocal relationships based on giving. In the experiment, subjects forage individually, experience variation in resource acquisition, and then consume either by actions in which resources are taken from, or moved to, others in a group environment. The key feature of the experimental design is that individuals can transfer resources to others, attempt to take resources from others and defend against take-away attempts. Many subjects begin by attempting to take resources from others, who can resist those attempts at a cost to each. Over time, subjects shift to a cooperative strategy of voluntary reciprocal giving, a response not suggested by the instructions. These results provide evidence that people are independently able to overcome initial use of taking strategies, evaluate gains from exchange, and create endogenous reciprocal trading relationships as a response to unsynchronized variance in resource availability.

Greater wealth inequality, less polygyny: rethinking the polygyny threshold model.

Monogamy appears to have become the predominant human mating system with the emergence of highly unequal agricultural populations that replaced relatively egalitarian horticultural populations, challenging the conventional idea-based on the polygyny threshold model-that polygyny should be positively associated with wealth inequality. To address this polygyny paradox, we generalize the standard polygyny threshold model to a mutual mate choice model predicting the fraction of women married polygynously. We then demonstrate two conditions that are jointly sufficient to make monogamy the predominant marriage form, even in highly unequal societies. We assess if these conditions are satisfied using individual-level data from 29 human populations. Our analysis shows that with the shift to stratified agricultural economies: (i) the population frequency of relatively poor individuals increased, increasing wealth inequality, but decreasing the frequency of individuals with sufficient wealth to secure polygynous marriage, and (ii) diminishing marginal fitness returns to additional wives prevent extremely wealthy men from obtaining as many wives as their relative wealth would otherwise predict. These conditions jointly lead to a high population-level frequency of monogamy.