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.

Common Features of Environmental Mycobacterium chelonae from Colorado Using Partial and Whole Genomic Sequence Analyses.

Nontuberculous mycobacteria (NTM) are environmentally acquired opportunistic pathogens that cause chronic lung disease in susceptible individuals. While presumed to be ubiquitous in built and natural environments, NTM environmental studies are limited. While environmental sampling campaigns have been performed in geographic areas of high NTM disease burden, NTM species diversity is less defined among areas of lower disease burden like Colorado. In Colorado, metals such as molybdenum have been correlated with increased risk for NTM infection, yet environmental NTM species diversity has not yet been widely studied. Based on prior regression modeling, three areas of predicted high, moderate, and low NTM risk were identified for environmental sampling in Colorado. Ice, plumbing biofilms, and sink tap water samples were collected from publicly accessible freshwater sources. All samples were microbiologically cultured and NTM were identified using partial rpoB gene sequencing. From these samples, areas of moderate risk were more likely to be NTM positive. NTM recovery from ice was more common than recovery from plumbing biofilms or tap water. Overall, nine different NTM species were identified, including clinically important Mycobacterium chelonae. MinION technology was used to whole genome sequence and compare mutational differences between six M. chelonae genomes, representing three environmental isolates from this study and three other M. chelonae isolates from other sources. Drug resistance genes and prophages were common findings among environmentally derived M. chelonae, promoting the need for expanded environmental sampling campaigns to improve our current understanding of NTM species abundance while opening new avenues for improved targeted drug therapies.

Surmounting the off-flavor challenge in plant-based foods.

Plant-based food products have been receiving an astronomical amount of attention recently, and their demand will most likely soar in the future. However, their unpleasant, intrinsic flavor and odor are the major obstacles limiting consumer's acceptance. These off-flavors are often described as "green," "grassy," "beany," "fatty" and "bitter." This review highlights the presence and formation of common off-flavor volatiles (aldehydes, alcohols, ketones, pyrazines, furans) and nonvolatiles (phenolics, saponins, peptides, alkaloids) from a variety of plant-based foods, including legumes (e.g. lentil, soy, pea), fruits (e.g. apple, grape, watermelon) and vegetables (e.g. carrot, potato, radish). These compounds are formed through various pathways, including lipid oxidation, ethanol fermentation and Maillard reaction (and Strecker degradation). The effect of off-flavor compounds as received by the human taste receptors, along with its possible link of bioactivity (e.g. anti-inflammatory effect), are briefly discussed on a molecular level. Generation of off-flavor compounds in plants is markedly affected by the species, cultivar, geographical location, climate conditions, farming and harvest practices. The effects of genome editing (i.e. CRISPR-Cas9), various processing technologies, such as antioxidant supplementation, enzyme treatment, extrusion, fermentation, pressure application, and different storage and packaging conditions, have been increasingly studied in recent years to mitigate the formation of off-flavors in plant foods. The information presented in this review could be useful for agricultural practitioners, fruits and vegetables industry, and meat and dairy analogue manufacturers to improve the flavor properties of plant-based foods.

Anthocyanins-gut microbiota-health axis: A review.

Anthocyanins are a subclass of flavonoids responsible for color in some fruits and vegetables with potent antioxidative capacity. During digestion, a larger proportion of dietary anthocyanins remains unabsorbed and reach the large intestine where they interact with the gut microbiota. Anthocyanins can modulate gut microbial populations to improve diversity and the proportion of beneficial populations, leading to alterations in short chain fatty acid and bile acid production. Some anthocyanins can be degraded into colonic metabolites, such as phenolic acids, which accumulate in the body and regulate a range of biological activities. Here we provide an overview of the effects of dietary anthocyanin consumption on gut microbial interactions, metabolism, and composition. Progression of chronic diseases has been strongly associated with imbalances in gut microbial populations. We therefore focus on the role of the gut microbiota as the 'mediator' that facilitates the therapeutic potential of anthocyanins against various chronic diseases, including obesity, type II diabetes, cardiovascular disease, neurodegenerative disease, inflammatory bowel disease, cancer, fatty liver disease, chronic kidney disease and osteoarthritis.

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.

Tyramine-derived hydroxycinnamic acid amides in plant foods: sources, synthesis, health effects and potential applications in food industry.

Tyramine-derived hydroxycinnamic acid amines (HCAAT) are naturally occurring group of secondary metabolites present in various plant genera, such as Allium, Cannabis, Lycium, Polyganotum and Solanum. It belongs to the neutral, water-insoluble compounds and plays a role in plant growth, development and defence mechanism. The past two decades have seen a shift in the study of HCAAT from its role in plants to its potent biological activities. This review highlights the sources, roles in plants, biosynthetic pathways, metabolic engineering and chemical synthesis of HCAAT. The biological properties of HCAAT remain the focus in this paper, including antioxidant, anti-inflammatory, anti-cancer, anti-diabetic, anti-melanogenesis and neuroprotective properties. The effects of food processing and technology on HCAAT are also discussed. Given the current research gap, this review proposes future directions on the study of HCAAT, as well as its potential applications in food and pharmaceutical industry.

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.

Lignanamides: sources, biosynthesis and potential health benefits - a minireview.

Lignanamides are natural plant secondary metabolites derived from oxidative coupling mechanism with hydroxycinnamic acid amides as intermediates. These compounds display powerful anti-inflammatory, antioxidant, anti-cancer and anti-hyperlipidemic capacities in vitro, cell culture and in vivo studies. With strong potential to be utilized as protective agents against human chronic diseases, these compounds have attracted the interest of researchers. This review aims to discuss current understanding on the sources, classification, biosynthesis of lignanamides in plants, and importantly their biological activity and potential health benefits. The general biosynthesis pathway for lignanamides is comprehensively summarized, though some details in molecular regulation of the coupling process have yet to be elucidated. Lignanamides deserves additional clinical studies involving animal and human subjects, to prove its health benefits.

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.

Hydroxycinnamic acids on gut microbiota and health.

Hydroxycinnamic acids (HCAs) are a major class of phenolic acids with the characteristic phenylpropanoid C6 -C3 backbone. Its typically conjugated status with plant cell wall components and liberation by limited enzymes might be the reason for its neglect by researchers compared to flavonoid-type polyphenols. The polyphenol-gut microbiota interactions and their impact on human health have captured the interest of researchers recently. In addition, there has been a significant progress over the past few years in understanding the gut microbiota-modulating effect of HCA using animal model studies. This review discusses the metabolism of HCA in the digestive tract, HCA-gut microbiota interactions, and its link to colorectal cancer, inflammatory bowel diseases, mental-cognitive impairments, nonalcoholic liver disease, and obesity. The effects of food matrix and processing technologies on HCA bioavailability and HCA-gut microbiota interactions, and HCA safety concerns are also featured in this review. This paper has provided an in-depth insight on HCA-gut microbiota relationship and identified the current literature gaps for future research.

Application of extrusion technology in plant food processing byproducts: An overview.

The food processing industry generates an immense amount of waste, which leads to major concerns for its environmental impact. However, most of these wastes, such as plant-derived byproducts, are still nutritionally adequate for use in food manufacturing. Extrusion is one of the most versatile and commercially successful processing technologies, with its widespread applications in the production of pasta, snacks, crackers, and meat analogues. It allows a high degree of user control over the processing parameters that significantly alters the quality of final products. This review features the past research on manufacture of extruded foods with integration of various plant food processing byproducts. The impact of extrusion parameters and adding various byproducts on the nutritional, physicochemical, sensory, and microbiological properties of food products are comprehensively discussed. This paper also provides fundamental knowledge and practical techniques for food manufacturers and researchers on the extrusion processing of plant food byproducts, which may increase economical return to the industry and reduce the environmental impact.

Hempseed in food industry: Nutritional value, health benefits, and industrial applications.

Hemp (Cannabis sativa L.) seeds have been consumed in Asian communities since prehistoric times. Recently, Australia, Canada, and the United States have legalized the cultivation and consumption of hempseed at low (<0.3%) tetrahydrocannabinol levels, and there's a growing interest in hempseed due to its nutritional value and pharmaceutical potential. This review aims to summarize the chemical composition, nutritional value, and potential health benefits of hempseed, as researched via in vitro and in vivo trials. The application of hempseed in the food industry is limited due to its poor performance on some functional properties, so the latest processing methods developed to improve these properties were compared. Additionally, manufacturing technologies incorporating hemp seeds into existing food products are also elaborated. This review would promote further in-depth research on this recently approved food resources and maximize its utilization in new food product development.

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.

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.

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.

Birth seasons and heights among girls and boys below 12 years of age: lasting effects and catch-up growth among native Amazonians in Bolivia.

BACKGROUND: Seasons affect many social, economic, and biological outcomes, particularly in low-resource settings, and some studies suggest that birth season affects child growth. AIM: To study a predictor of stunting that has received limited attention: birth season. SUBJECTS AND METHODS: This study uses cross-sectional data collected during 2008 in a low-resource society of horticulturists-foragers in the Bolivian Amazon, Tsimane'. It estimates the associations between birth months and height-for-age Z-scores (HAZ) for 562 girls and 546 boys separately, from birth until age 11 years or pre-puberty, which in this society occurs ∼13-14 years. RESULTS: Children born during the rainy season (February-May) were shorter, while children born during the end of the dry season and the start of the rainy season (August-November) were taller, both compared with their age-sex peers born during the rest of the year. The correlations of birth season with HAZ were stronger for boys than for girls. Controlling for birth season, there is some evidence of eventual partial catch-up growth, with the HAZ of girls or boys worsening until ∼ age 4-5 years, but improving thereafter. By age 6 years, many girls and boys had ceased to be stunted, irrespective of birth season. CONCLUSION: The results suggest that redressing stunting will require attention to conditions in utero, infancy and late childhood.

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.