Pearl Memorial Lecture. Humans at the extremes: Exploring human adaptation to ecological and social stressors.

The field of human biology has long explored how human populations have adapted to extreme environmental circumstances. Yet, it has become increasingly clear that conditions of social stress, poverty, and lifestyle change play equally important roles in shaping human biological variation and health. In this paper, I provide a brief background on the foundational human adaptability research of the International Biological Programme (IBP) from the 1960s, highlighting how its successes and critiques have shaped current research directions in the field. I then discuss and reflect on my own field research that has examined the influence of both environmental and social stresses on human populations living in different ecosystems: the Peruvian Andes, the Siberian arctic, and the Bolivian rainforest. Finally, I consider how the papers in this special issue advance our understanding of human adaptability to extreme conditions and offer directions for future research. Drawing on our field's distinctive evolutionary and biocultural perspectives, human biologists are uniquely positioned to examine how the interplay between social and ecological domains influences the human condition.

Variability in energy expenditure is much greater in males than females.

In mammals, trait variation is often reported to be greater among males than females. However, to date, mainly only morphological traits have been studied. Energy expenditure represents the metabolic costs of multiple physical, physiological, and behavioral traits. Energy expenditure could exhibit particularly high greater male variation through a cumulative effect if those traits mostly exhibit greater male variation, or a lack of greater male variation if many of them do not. Sex differences in energy expenditure variation have been little explored. We analyzed a large database on energy expenditure in adult humans (1494 males and 3108 females) to investigate whether humans have evolved sex differences in the degree of interindividual variation in energy expenditure. We found that, even when statistically comparing males and females of the same age, height, and body composition, there is much more variation in total, activity, and basal energy expenditure among males. However, with aging, variation in total energy expenditure decreases, and because this happens more rapidly in males, the magnitude of greater male variation, though still large, is attenuated in older age groups. Considerably greater male variation in both total and activity energy expenditure could be explained by greater male variation in levels of daily activity. The considerably greater male variation in basal energy expenditure is remarkable and may be explained, at least in part, by greater male variation in the size of energy-demanding organs. If energy expenditure is a trait that is of indirect interest to females when choosing a sexual partner, this would suggest that energy expenditure is under sexual selection. However, we present a novel energetics model demonstrating that it is also possible that females have been under stabilizing selection pressure for an intermediate basal energy expenditure to maximize energy available for reproduction.

The evolutionary significance of human brown adipose tissue: Integrating the timescales of adaptation.

While human adaptability is regarded as a classical topic in anthropology, recent work provides new insight into metabolic adaptations to cold climates and the role of phenotypic plasticity in human evolution. A growing body of literature demonstrates that adults retain brown adipose tissue (BAT) which may play a role in non-shivering thermogenesis. In this narrative review, we apply the timescales of adaptation framework in order to explore the adaptive significance of human BAT. Human variation in BAT is shaped by multiple adaptive modes (i.e., allostasis, acclimatization, developmental adaptation, epigenetic inheritance, and genetic adaptation), and together the adaptive modes act as an integrated system. We hypothesize that plasticity in BAT facilitated the successful expansion of human populations into circumpolar regions, allowing for selection of genetic adaptations to cold climates to take place. Future research rooted in human energetics and biocultural perspectives is essential for understanding BAT's adaptive and health significance.

Brown adipose tissue thermogenesis among young adults in northeastern Siberia and Midwest United States and its relationship with other biological adaptations to cold climates.

OBJECTIVES: Recent research suggests that brown adipose tissue (BAT) plays a functional role in non-shivering thermogenesis; however, few studies have examined population variation in BAT or its relationship with other mechanisms of adaptation to cold stress. This study characterized BAT thermogenesis and other adaptive responses to low temperatures among Indigenous Siberian young adults and young adults living near Chicago, IL. MATERIALS AND METHODS: We recruited 72 Yakut participants (42 females; 30 males) and 54 participants in Evanston, IL (40 females; 14 males). Anthropometric dimensions and resting metabolic rate (RMR) were measured, and we calculated percent divergence in RMR from expected values (divRMR). We also quantified change in supraclavicular temperature, sternum temperature, and energy expenditure after a mild cooling condition. RESULTS: Participants in Yakutia were less likely to shiver during the cooling condition (p < .05) and exhibited significantly greater evidence of BAT thermogenesis, warmer sternum temperatures, and higher divRMR than participants in Evanston (p < .05). Additionally, the relationship between change in supraclavicular temperature and energy expenditure differed between the two samples. CONCLUSIONS: Yakut young adults displayed greater evidence of BAT thermogenesis in response to mild cooling compared with young adults living near Chicago, IL. Furthermore, the relationship between BAT thermogenesis and change in energy expenditure appears to be stronger among Yakut adults. Adults that exhibited greater metabolic response to cold stress, such as higher BAT thermogenesis and divRMR, maintained warmer sternum temperatures. These results highlight the degree to which adaptation to cold climates involves multiple integrated biological pathways.

Evidence for a sensitive period of plasticity in brown adipose tissue during early childhood among indigenous Siberians.

OBJECTIVES: Evolutionary theorists have debated the adaptive significance of developmental plasticity in organisms with long lifespans such as humans. This debate in part stems from uncertainty regarding the timing of sensitive periods. Does sensitivity to environmental signals fluctuate across development or does it steadily decline? We investigated developmental plasticity in brown adipose tissue (BAT) among indigenous Siberians in order to explore the timing of phenotypic sensitivity to cold stress. METHODS: BAT thermogenesis was quantified using infrared thermal imaging in 78 adults (25 men; 33 women). Cold exposure during gestation, infancy, early childhood, middle childhood, and adolescence was quantified using: (1) the average ambient temperature across each period; (2) the number of times daily temperature dropped below -40°F during each period. We also assessed past cold exposure with a retrospective survey of participation in outdoor activities. RESULTS: Adult BAT thermogenesis was significantly associated with the average temperature (p = 0.021), the number of times it was below -40°F (p = 0.026), and participation in winter outdoor activities (p = 0.037) during early childhood. CONCLUSIONS: Our results suggest that early childhood represents an important stage for developmental plasticity, and that culture may play a critical role in shaping the timing of environmental signals. The findings highlight a new pathway through which the local consequences of global climate change may influence human biology, and they suggest that ambient temperature may represent an understudied component of the developmental origins of health and disease.

Influence of nutritional status on basal metabolic rates among rural agriculturalists of Ngilo-Ilo, East Java.

OBJECTIVES: Previous research has shown that tropical island populations have reduced basal metabolic rates (BMR) associated with the joint influences of heat stress and undernutrition. This study examines variation in BMR among an indigenous population of Indonesia, and compares these data with those collected from earlier studies in Indonesia. METHODS: Anthropometric dimensions and BMR were measured on a sample of 35 Indonesian adults (28 men, 7 women) from the rural village of Ngilo-Ilo, East Java. RESULTS: Mean measured BMRs (±SD) were 1433 ± 344 kcal/d in men and 1256 ±257 kcal/d in women, and were not significantly different from estimates using the FAO/WHO/UNU predictive questions. Underweight individuals (BMIs <18.5 kg/m2 ) had BMRs that were 7.6% below predicted levels, while those with BMIs ≥18.5 kg/m2 had BMRs that were 8.0% above predicted levels (P < .01). Underweight individuals also had significantly higher respiratory quotients (RQ = .94 vs. .89; P < .05), suggesting lower levels of fat oxidation. Compared to data from previous studies (1929-1979), men of the Ngilo-Ilo sample had similar BMIs (19.8 vs. 19.2 kg/m2 ), but higher BMRs, after adjusting for age and body weight (+2.1% vs. -5.6%; P < .05). CONCLUSIONS: Among the agriculturalists of Ngilo-Ilo, measured BMRs were low, but not significantly different from those predicted by the FAO/WHO/UNU equations. Among subjects of this sample and from earlier studies, poorer physical nutritional status was associated with reduced BMRs. These results suggest that chronic energy stress has consistently shaped metabolic function among Indonesian rural populations.

Child stunting is associated with weaker human capital among native Amazonians.

OBJECTIVES: We assessed associations between child stunting, recovery, and faltering with schooling and human capital skills in a native Amazonian society of horticulturalists-foragers (Tsimane'). METHODS: We used cross-sectional data (2008) from 1262 children aged 6 to 16 years in 53 villages to assess contemporaneous associations between three height categories: stunted (height-for-age Z score, HAZ<-2), moderately stunted (-2 ≤ HAZ≤-1), and nonstunted (HAZ>-1), and three categories of human capital: completed grades of schooling, test-based academic skills (math, reading, writing), and local plant knowledge. We used annual longitudinal data (2002-2010) from all children (n = 853) in 13 villages to estimate the association between changes in height categories between the first and last years of measure and schooling and academic skills. RESULTS: Stunting was associated with 0.4 fewer completed grades of schooling (∼24% less) and with 13-15% lower probability of showing any writing or math skills. Moderate stunting was associated with ∼20% lower scores in local plant knowledge and 9% lower probability of showing writing skills, but was not associated with schooling or math and writing skills. Compared with nonstunted children, children who became stunted had 18-21% and 15-21% lower probabilities of showing math and writing skills, and stunted children had 0.4 fewer completed grades of schooling. Stunted children who recovered showed human capital outcomes that were indistinguishable from nonstunted children. CONCLUSIONS: The results confirm adverse associations between child stunting and human capital skills. Predictors of growth recovery and faltering can affect human capital outcomes, even in a remote, economically self-sufficient society.

Brown adipose tissue, energy expenditure, and biomarkers of cardio-metabolic health among the Yakut (Sakha) of northeastern Siberia.

OBJECTIVES: This study provides the first investigation of non-shivering thermogenesis (NST) and brown adipose tissue (BAT) activity among an indigenous circumpolar population, the Yakut of northeastern Siberia. The study also examines the health significance of BAT activity in this population by testing the relationships between BAT thermogenesis and biomarkers of cardio-metabolic disease risk, such as percent body fat and blood glucose and cholesterol levels. METHODS: Data were collected in the Sakha Republic (Yakutia) for 31 men and 43 women. Change in energy expenditure and BAT thermogenesis were quantified after a 30-minute mild cooling condition. Anthropometric dimensions, blood glucose, and lipid levels were also collected. RESULTS: On average, the skin temperature of the supraclavicular area was constant after cooling while the skin temperature of a point on the sternum dropped significantly (P < .001), thus suggesting the presence of active supraclavicular BAT among Yakut adults. Participants with evidence of greater BAT thermogenesis exhibited a larger percent change in energy expenditure (% ΔEE) and an increase in respiratory quotient (RQ) after cooling (P ≤ .05). While there was no relationship between BAT activity and blood lipid levels, BAT thermogenesis was positively associated with blood glucose levels (P < .01). CONCLUSIONS: Yakut adults exhibit evidence of active BAT deposits. Given that there is a significant relationship between BAT activity and % ΔEE, it is possible that BAT plays a role in NST among Yakut adults. While the relationship between BAT and body composition is inconclusive, participants with greater BAT seemed to preferentially utilize glucose during cold stress exposure.

Metabolic costs and evolutionary implications of human brain development.

The high energetic costs of human brain development have been hypothesized to explain distinctive human traits, including exceptionally slow and protracted preadult growth. Although widely assumed to constrain life-history evolution, the metabolic requirements of the growing human brain are unknown. We combined previously collected PET and MRI data to calculate the human brain's glucose use from birth to adulthood, which we compare with body growth rate. We evaluate the strength of brain-body metabolic trade-offs using the ratios of brain glucose uptake to the body's resting metabolic rate (RMR) and daily energy requirements (DER) expressed in glucose-gram equivalents (glucosermr% and glucoseder%). We find that glucosermr% and glucoseder% do not peak at birth (52.5% and 59.8% of RMR, or 35.4% and 38.7% of DER, for males and females, respectively), when relative brain size is largest, but rather in childhood (66.3% and 65.0% of RMR and 43.3% and 43.8% of DER). Body-weight growth (dw/dt) and both glucosermr% and glucoseder% are strongly, inversely related: soon after birth, increases in brain glucose demand are accompanied by proportionate decreases in dw/dt. Ages of peak brain glucose demand and lowest dw/dt co-occur and subsequent developmental declines in brain metabolism are matched by proportionate increases in dw/dt until puberty. The finding that human brain glucose demands peak during childhood, and evidence that brain metabolism and body growth rate covary inversely across development, support the hypothesis that the high costs of human brain development require compensatory slowing of body growth rate.

Lifestyle mediates seasonal changes in metabolic health among the yakut (sakha) of northeastern siberia.

OBJECTIVES: Among indigenous circumpolar populations, extreme seasonality influences food availability and energy metabolism. Furthermore, subsistence patterns and wage labor opportunities shift with season. Thus, health measures among circumpolar populations likely exhibit seasonal changes that are influenced by lifestyle factors. This study examines how markers of cardio-metabolic health vary between summer and winter as a function of an individual's lifestyle and sex among the Yakut of northeastern Siberia. METHODS: Anthropometric dimensions, serum lipids and glucose levels, blood pressure, and lifestyle data were collected for a sample of 115 Yakut participants (71 women, 44 men) in Berdygestiakh, Sakha Republic, Russia in the summer of 2009 and winter of 2011. RESULTS: Men and women experienced significant increases in total and HDL cholesterol and triglyceride levels from summer to winter. Women exhibited winter-time increases in adiposity and glucose levels. Men who reported greater market integration were more likely to have lower winter blood pressure levels. Additionally, time spent fishing was associated with lower winter-time LDL cholesterol, while foraging time was associated with higher HDL cholesterol. CONCLUSIONS: While seasonal changes in anthropometric dimensions were modest, Yakut men and women experienced significant increases in total cholesterol and HDL cholesterol from summer to winter. These results also suggest that while Yakut individuals with greater subsistence participation are more buffered from adverse seasonal changes in cholesterol levels, they may be at a greater risk for winter increases in blood pressure. Furthermore, the interactions between lifestyle and seasonal change in metabolic health appear to differ between Yakut women and men. Am. J. Hum. Biol. 28:868-878, 2016. © 2016Wiley Periodicals, Inc.

Adiponectin, hemoglobin, and cardiovascular risk in an indigenous siberian population.

OBJECTIVES: Adipose tissue hypoxia appears to play a role in promoting chronic inflammation and the development of obesity-related cardiovascular and metabolic diseases, yet the underlying mechanisms are not well understood. The aim of the present research is to examine whether adiponectin levels (an adipocyte-derived hormone with anti-inflammatory properties) are inversely correlated with hemoglobin levels in an indigenous Siberian population. METHODS: The study was conducted among 252 Yakut adults (≥18 years; 135 females) from Berdygestiakh, Sakha Republic, Russia. Measurements included anthropometric dimensions (body mass index [BMI], waist circumference [WC], and percent body fat) and blood levels of hemoglobin and adiponectin. RESULTS: Yakut females had higher adiponectin concentrations than males (15.1 ± 9.8 vs. 11.7 ± 10.6 µg/ml; P < 0.001), whereas males had higher hemoglobin levels (14.4 ± 1.4 vs. 12.6 ± 1.5 g/dL; P < 0.001). Body composition measures in both sexes were negatively associated with adiponectin and positively associated with hemoglobin. After adjusting for central adiposity and smoking, adiponectin levels were negatively correlated with hemoglobin levels in men (P < 0.05), but not in women (P = 0.511). CONCLUSIONS: This investigation provides some support for the involvement of hypoxia-related dysregulation of adiponectin associated with obesity and potentially cardiovascular disease. Am. J. Hum. Biol. 28:580-583, 2016. © 2015 Wiley Periodicals, Inc.

Catch-up growth and growth deficits: Nine-year annual panel child growth for native Amazonians in Bolivia.

BACKGROUND: Childhood growth stunting is negatively associated with cognitive and health outcomes, and is claimed to be irreversible after age 2. AIM: To estimate growth rates for children aged 2-7 who were stunted (sex-age standardised z-score [HAZ] <-2), marginally-stunted (-2 ≤ HAZ ≤-1) or not-stunted (HAZ >-1) at baseline and tracked annually until age 11; frequency of movement among height categories; and variation in height predicted by early childhood height. SUBJECTS AND METHODS: This study used a 9-year annual panel (2002-2010) from a native Amazonian society of horticulturalists-foragers (Tsimane'; n = 174 girls; 179 boys at baseline). Descriptive statistics and random-effect regressions were used. RESULTS: This study found some evidence of catch-up growth in HAZ, but persistent height deficits. Children stunted at baseline improved 1 HAZ unit by age 11 and had higher annual growth rates than non-stunted children. Marginally-stunted boys had a 0.1 HAZ units higher annual growth rate than non-stunted boys. Despite some catch up, ∼ 80% of marginally-stunted children at baseline remained marginally-stunted by age 11. The height deficit increased from age 2 to 11. Modest year-to-year movement was found between height categories. CONCLUSIONS: The prevalence of growth faltering among the Tsimane' has declined, but hurdles still substantially lock children into height categories.

Socio-demographic predictors of sleep complaints in indigenous Siberians with a mixed economy.

OBJECTIVES: Socio-demographic indicators closely relate to sleep in industrialized populations. However we know very little about how such factors impact sleep in populations undergoing industrialization. Within populations transitioning to the global economy, the preliminary evidence has found an inconsistent relationship between socio-demographics and sleep complaints across countries and social strata. MATERIALS AND METHODS: Surveys were conducted on a sample of rural Sakha (Yakut) adults (n = 168) during the autumn of 2103 to assess variation in socio-demographics and sleep complaints, including trouble sleeping and daytime sleepiness. Socio-demographic variables included age, gender, socioeconomic measures, and markers of traditional/market-based lifestyle. We tested whether the socio-demographic variables predicted sleep complaints using bivariate analyses and multiple logistic regressions. RESULTS: Trouble sleeping was reported by 18.5% of the participants and excessive daytime sleepiness (EDS) by 17.3%. Trouble sleeping was significantly predicted by older age, female gender, and mixing traditional and market-based lifestyles. EDS was not significantly predicted by any socio-demographic variable. DISCUSSION: These findings support the few large-scale studies that found inconsistent relationships between measures of socioeconomic status and sleep complaints in transitioning populations. Employing a mix of traditional and market-based lifestyles may leave Sakha in a space of vulnerability, leading to trouble sleeping.

Do physical activity and sedentary behavior relate to cardio-metabolic risk factor clustering in indigenous Siberian adults?

OBJECTIVES: To investigate whether having multiple risk factors for cardio-metabolic disease is associated with objectively measured physical activity or sedentary behavior within a sample of Yakut (Sakha) of Siberia. METHODS: This cross sectional study involved 63 Yakut adults (32 men) who were measured for cardio-metabolic risk factors. Free living physical activity and sedentary behavior were calculated from waist accelerometry. Correlations and t-tests were used to assess the relationship between moderate-vigorous physical activity (MVPA), sedentary behavior (SB), and individual risk factors and clustering of risk factors. RESULTS: These Yakut were physically active, with 54.4% spending at least 30 min in MVPA, with men being more active than women and women having less favorable cardio-metabolic profiles. These Yakut spent about 7.5 h in SB a day. SB was not related to cardio-metabolic risk factors. MVPA was significantly and negatively related to waist circumference and risk factor clustering in men and the total sample. MVPA was not related to women's risk factors. CONCLUSIONS: Objectively measured physical activity was related to lower risk of cardio-metabolic risk factor clustering within this sample of Yakut men, but not women. SB was not related to cardio-metabolic indicators. Physical activity may contribute to a reduction in clustering of metabolic risk factors within indigenous circumpolar populations.