Benjamin C. Trumble

Coronary atherosclerosis in indigenous South American Tsimane: a cross-sectional cohort study

BACKGROUNDnConventional coronary artery disease risk factors might potentially explain at least 90% of the attributable risk of coronary artery disease. To better understand the association between the pre-industrial lifestyle and low prevalence of coronary artery disease risk factors, we examined the Tsimane, a Bolivian population living a subsistence lifestyle of hunting, gathering, fishing, and farming with few cardiovascular risk factors, but high infectious inflammatory burden.nnnMETHODSnWe did a cross-sectional cohort study including all individuals who self-identified as Tsimane and who were aged 40 years or older. Coronary atherosclerosis was assessed by coronary artery calcium (CAC) scoring done with non-contrast CT in Tsimane adults. We assessed the difference between the Tsimane and 6814 participants from the Multi-Ethnic Study of Atherosclerosis (MESA). CAC scores higher than 100 were considered representative of significant atherosclerotic disease. Tsimane blood lipid and inflammatory biomarkers were obtained at the time of scanning, and in some patients, longitudinally.nnnFINDINGSnBetween July 2, 2014, and Sept 10, 2015, 705 individuals, who had data available for analysis, were included in this study. 596 (85%) of 705 Tsimane had no CAC, 89 (13%) had CAC scores of 1-100, and 20 (3%) had CAC scores higher than 100. For individuals older than age 75 years, 31 (65%) Tsimane presented with a CAC score of 0, and only four (8%) had CAC scores of 100 or more, a five-fold lower prevalence than industrialised populations (p≤0·0001 for all age categories of MESA). Mean LDL and HDL cholesterol concentrations were 2·35 mmol/L (91 mg/dL) and 1·0 mmol/L (39·5 mg/dL), respectively; obesity, hypertension, high blood sugar, and regular cigarette smoking were rare. High-sensitivity C-reactive protein was elevated beyond the clinical cutoff of 3·0 mg/dL in 360 (51%) Tsimane participants.nnnINTERPRETATIONnDespite a high infectious inflammatory burden, the Tsimane, a forager-horticulturalist population of the Bolivian Amazon with few coronary artery disease risk factors, have the lowest reported levels of coronary artery disease of any population recorded to date. These findings suggest that coronary atherosclerosis can be avoided in most people by achieving a lifetime with very low LDL, low blood pressure, low glucose, normal body-mass index, no smoking, and plenty of physical activity. The relative contributions of each are still to be determined.nnnFUNDINGnNational Institute on Aging, National Institutes of Health; St Lukes Hospital of Kansas City; and Paleocardiology Foundation.

Apolipoprotein E4 is associated with improved cognitive function in Amazonian forager-horticulturalists with a high parasite burden

The apolipoprotein E4 (E4) allele is present worldwide, despite its associations with higher risk of cardiovascular morbidity, accelerated cognitive decline during aging, and Alzheimers disease (AD). The E4 allele is especially prevalent in some tropical regions with a high parasite burden. Equatorial populations also face a potential dual burden of high E4 prevalence combined with parasitic infections that can also reduce cognitive performance. We examined the interactions of E4, parasite burden, and cognitive performance in a traditional, nonindustrialized population of Amazonian forager‐horticulturalists (N = 372) to test whether E4 protects against cognitive decline in environments with a heavy pathogen burden. Contrary to observations in industrial pop‐ulations, older adult E4 carriers with high parasite burdens either maintained or showed slight improvements in cognitive performance, whereas non‐E4 carriers with a high parasite burden showed reduced cognitive performance. Being an E4 carrier is the strongest risk factor to date of AD and cognitive decline in industrial populations; it is associated with greater cognitive performance in individuals facing a high parasite and pathogen load, suggesting advantages to the E4 allele under certain environmental conditions. The current mismatch between postindustrial hygienic lifestyles and active parasite‐rich environs may be critical for understanding genetic risk for cognitive aging. —Trumble, B. C., Stieglitz, J., Blackwell, A. D., Allayee, H., Beheim, B., Finch, C. E., Gurven, M., Kaplan, H. Apolipoprotein E4 is associated with improved cognitive function in Amazonian forager‐horticulturalists with a high parasite burden. FASEB J. 31, 1508–1515 (2017) www.fasebj.org

The Tsimane health and life history project: Integrating anthropology and biomedicine

The Tsimane Health and Life History Project, an integrated bio‐behavioral study of the human life course, is designed to test competing hypotheses of human life‐history evolution. One aim is to understand the bidirectional connections between life history and social behavior in a high‐fertility, kin‐based context lacking amenities of modern urban life (e.g. sanitation, banks, electricity). Another aim is to understand how a high pathogen burden influences health and well‐being during development and adulthood. A third aim addresses how modernization shapes human life histories and sociality. Here we outline the projects goals, history, and main findings since its inception in 2002. We reflect on the implications of current findings and highlight the need for more coordinated ethnographic and biomedical study of contemporary nonindustrial populations to address broad questions that can situate evolutionary anthropology in a key position within the social and life sciences.

Cardiovascular disease and type 2 diabetes in evolutionary perspective: A critical role for helminths?

Heart disease and type 2 diabetes are commonly believed to be rare among contemporary subsistence-level human populations, and by extension prehistoric populations. Although some caveats remain, evidence shows these diseases to be unusual among well-studied hunter-gatherers and other subsistence populations with minimal access to healthcare. Here we expand on a relatively new proposal for why these and other populations may not show major signs of these diseases. Chronic infections, especially helminths, may offer protection against heart disease and diabetes through direct and indirect pathways. As part of a strategy to insure their own survival and reproduction, helminths exert multiple cardio-protective effects on their host through their effects on immune function and blood lipid metabolism. Helminths consume blood lipids and glucose, alter lipid metabolism, and modulate immune function towards Th-2 polarization—which combined can lower blood cholesterol, reduce obesity, increase insulin sensitivity, decrease atheroma progression, and reduce likelihood of atherosclerotic plaque rupture. Traditional cardiometabolic risk factors, coupled with the mismatch between our evolved immune systems and modern, hygienic environments may interact in complex ways. In this review, we survey existing studies in the non-human animal and human literature, highlight unresolved questions and suggest future directions to explore the role of helminths in the etiology of cardio-metabolic disease.

Horticultural activity predicts later localized limb status in a contemporary pre-industrial population

OBJECTIVESnModern humans may have gracile skeletons due to low physical activity levels and mechanical loading. Tests using pre-historic skeletons are limited by the inability to assess behavior directly, while modern industrialized societies possess few socio-ecological features typical of human evolutionary history. Among Tsimane forager-horticulturalists, we test whether greater activity levels and, thus, increased loading earlier in life are associated with greater later-life bone status and diminished age-related bone loss.nnnMATERIALS AND METHODSnWe used quantitative ultrasonography to assess radial and tibial status among adults aged 20+ years (meanu2009±u2009SD ageu2009=u200949u2009±u200915; 52% female). We conducted systematic behavioral observations to assess earlier-life activity patterns (mean time lag between behavioural observation and ultrasoundu2009=u200912 years). For a subset of participants, physical activity was again measured later in life, via accelerometry, to determine whether earlier-life time use is associated with later-life activity levels. Anthropometric and demographic data were collected during medical exams.nnnRESULTSnStructural decline with age is reduced for the tibia (female: -0.25 SDs/decade; male: 0.05 SDs/decade) versus radius (female: -0.56 SDs/decade; male: -0.20 SDs/decade), which is expected if greater loading mitigates bone loss. Time allocation to horticulture, but not hunting, positively predicts later-life radial status (βHorticulture u2009=u20090.48, pu2009=u20090.01), whereas tibial status is not significantly predicted by subsistence or sedentary leisure participation.nnnDISCUSSIONnPatterns of activity- and age-related change in bone status indicate localized osteogenic responses to loading, and are generally consistent with the logic of bone functional adaptation. Nonmechanical factors related to subsistence lifestyle moderate the association between activity patterns and bone structure.

Marital violence and fertility in a relatively egalitarian high-fertility population

Ultimate and proximate explanations of men’s physical intimate partner violence (IPV) against women have been proposed. An ultimate explanation posits that IPV is used to achieve a selfish fitness-relevant outcome, and predicts that IPV is associated with greater marital fertility. Proximate IPV explanations contain either complementary strategic components (for example, men’s desire for partner control), non-strategic components (for example, men’s self-regulatory failure), or both strategic and non-strategic components involving social learning. Consistent with an expectation from an ultimate IPV explanation, we find that IPV predicts greater marital fertility among Tsimané forager-horticulturalists of Bolivia (nu2009=u2009133 marriages, 105 women). This result is robust to using between- versus within-subject comparisons, and considering secular changes, reverse causality, recall bias and other factors (for example, women’s preference for high-status men who may be more aggressive than lower-status men). Consistent with a complementary expectation from a strategic proximate IPV explanation, greater IPV rate is associated with men’s attitudes favouring intersexual control. Neither men’s propensity for intrasexual physical aggression, nor men’s or women’s childhood exposure to family violence predict IPV rate. Our results suggest a psychological and behavioural mechanism through which men exert direct influence over marital fertility, which may manifest when spouses differ in preferred family sizes.A study of intimate partner violence among the Tsimané forager-horticulturalists of Bolivia finds evidence that male aggression is leveraged to increase marital fertility and a man’s individual fitness when spouses differ in preferred family size.

Parental hormones are associated with crop loss and family sickness following catastrophic flooding in lowland Bolivia

The physiology of fatherhood is a growing field of study, and variability in hormonal mediators of reproductive effort (e.g. testosterone, cortisol) can predict variability in paternal investment. Studies often find that lower testosterone levels are associated with increased paternal investment, though most studies are conducted under relatively stable ecological conditions. In this paper, we examine parental physiological correlates of crop loss and family health problems among Tsimane forager-horticulturalists following a catastrophic flood in lowland Bolivia. Immediately after a devastating 2014 flood that impacted >75% of Tsimane communities, we conducted structured interviews examining crop losses and morbidity, and collected saliva specimens from 421 parents (nu202f=u202f292 households) to analyze cortisol and testosterone. Over 98% of interviewees reported horticultural losses, with the average family losing 88% of their crops, while 80% of families reported flood-induced injuries or illnesses. Controlling for age, body mass index, and time of specimen collection, mens testosterone was negatively associated with both absolute cropland losses (Std. βu202f=u202f-0.16, pu202f=u202f0.037), and percent of cropland lost (Std. βu202f=u202f-0.16, pu202f=u202f0.040). Female testosterone was not associated with crop losses. Using the same control variables, both male and female cortisol was negatively associated with a composite measure of child health burden (fathers: Std. βu202f=u202f-0.34, pu202f<u202f0.001; mothers: Std. βu202f=u202f-0.23, pu202f=u202f0.037). These results are discussed in the cultural context of a strong sexual division of labor among Tsimane; we highlight the physiological and psychosocial costs of experiencing a natural disaster, especially for paternal caregivers in a nutritionally and pathogenically stressed subsistence population where cultigens provide the majority of calories in the diet.

Child nutritional status among births exceeding ideal family size in a high fertility population

Ideal family size (IFS) is measured in social surveys to indicate unmet need for contraception and impending shifts in fertility behaviour. Whether exceeding IFS affects parental behaviour in ways that result in lower investments in child nutrition, well-being, and educational attainment is not known. This study examines parental IFS and the association between exceeding stated ideals and child nutritional status in a high-fertility, high-mortality population in the Bolivian Amazon. Height-for-age z-scores, weight-for-age z-scores, weight-for-height z-scores, stunting, haemoglobin, and anaemia status in 638 children aged 0-5xa0years are predicted as a function of birth order in relation to parental IFS, adjusting for household characteristics and mother and child random effects. Children of birth orders above paternal IFS experience higher weight-for-age z-scores when living further away from the market town of San Borja, consistent with underlying motivations for higher IFS and lower human capital investment in children in more remote areas (βxa0=xa0.009, pxa0=xa0.027). Overall, we find no statistical evidence that birth orders in excess of parental ideals are associated with compromised child nutrition below age 2, a period of intensive breastfeeding in this population. Despite a vulnerability to nutritional deficiencies postweaning for children age 2-5, there was no association between birth order in excess of parental ideals and lower nutritional status. Further studies examining this association at various stages of the fertility transition will elucidate whether reported ideal or optimal family sizes are flexible as trade-offs between quality and quantity of children shift during the transition to lower fertility.

Group-level competition influences urinary steroid hormones among wild red-tailed monkeys, indicating energetic costs

Various theories emphasize that intergroup competition should affect intragroup cooperation and social relationships, especially if the cost of intergroup competition outweighs that of intragroup competition. This cost of intergroup competition may be quantified by changes in physiological status, such as in the steroid hormones cortisol (C) and testosterone (T), which rise or are depressed during periods of energetic stress, respectively. Here we tested for changes in urinary C and T after intergroup encounters (IGEs) among wild red‐tailed monkeys (Cercopithecus ascanius), a species that experiences frequent intergroup feeding competition, at the Ngogo station in Kibale National Park, Uganda. We assayed 108 urine samples, of which 36 were collected after IGEs, from 23 individuals in four social groups. Bayesian multilevel models controlling for various confounds revealed that IGEs increased C and decreased T relative to baseline, consistent with an energetic cost to IGEs. The C change was more apparent in samples collected early after IGEs, suggesting an anticipatory increase, whereas the T change was stronger in later samples, suggesting sustained energetic trade‐offs. Hormone responses were not affected by the IGE outcome. This cost to intergroup competition, together with little evidence for intragroup competition in redtails and other guenons, establishes an interesting test case for theories emphasizing the effect of intergroup competition on intragroup cooperation.