Traditional Human Populations and Nonhuman Primates Show Parallel Gut Microbiome Adaptations to Analogous Ecological Conditions.

Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates. This overlap is thought to be driven by analogous dietary triggers; however, the ecological and functional bases of this similarity are not fully understood. To start addressing this issue, fecal metagenomes of BaAka hunter-gatherers and traditional Bantu agriculturalists from the Central African Republic were profiled and compared with those of a sympatric western lowland gorilla group (Gorilla gorilla gorilla) across two seasons of variable dietary intake. Results show that gorilla gut microbiomes shared similar functional traits with each human group, depending on seasonal dietary behavior. Specifically, parallel microbiome traits were observed between hunter-gatherers and gorillas when the latter consumed more structural polysaccharides during dry seasons, while small-scale agriculturalist and gorilla microbiomes showed significant functional overlap when gorillas consumed more seasonal ripe fruit during wet seasons. Notably, dominance of microbial transporters, transduction systems, and gut xenobiotic metabolism was observed in association with traditional agriculture and energy-dense diets in gorillas at the expense of a functional microbiome repertoire capable of metabolizing more complex polysaccharides. Differential abundance of bacterial taxa that typically distinguish traditional from industrialized human populations (e.g., Prevotella spp.) was also recapitulated in the human and gorilla groups studied, possibly reflecting the degree of polysaccharide complexity included in each group's dietary niche. These results show conserved functional gut microbiome adaptations to analogous diets in small-scale human populations and nonhuman primates, highlighting the role of plant dietary polysaccharides and diverse environmental exposures in this convergence.IMPORTANCE The results of this study highlight parallel gut microbiome traits in human and nonhuman primates, depending on subsistence strategy. Although these similarities have been reported before, the functional and ecological bases of this convergence are not fully understood. Here, we show that this parallelism is, in part, likely modulated by the complexity of plant carbohydrates consumed and by exposures to diverse xenobiotics of natural and artificial origin. Furthermore, we discuss how divergence from these parallel microbiome traits is typically associated with adverse health outcomes in human populations living under culturally westernized subsistence patterns. This is important information as we trace the specific dietary and environmental triggers associated with the loss and gain of microbial functions as humans adapt to various dietary niches.

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints.

The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets.IMPORTANCE The results of this study indicate a discordance between gut microbiome composition and evolutionary history in primates, calling into question previous notions about host genetic control of the primate gut microbiome. Microbiome similarities between humans consuming nonindustrialized diets and monkeys characterized by subsisting on eclectic, omnivorous diets also raise questions about the ecological and nutritional drivers shaping the human gut microbiome. Moreover, a more detailed understanding of the factors associated with gut microbiome plasticity in primates offers a framework to understand why humans following industrialized lifestyles have deviated from states thought to reflect human evolutionary history. The results also provide perspectives for developing therapeutic dietary manipulations that can reset configurations of the gut microbiome to potentially improve human health.

Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns.

To understand how the gut microbiome is impacted by human adaptation to varying environments, we explored gut bacterial communities in the BaAka rainforest hunter-gatherers and their agriculturalist Bantu neighbors in the Central African Republic. Although the microbiome of both groups is compositionally similar, hunter-gatherers harbor increased abundance of Prevotellaceae, Treponema, and Clostridiaceae, while the Bantu gut microbiome is dominated by Firmicutes. Comparisons with US Americans reveal microbiome differences between Africans and westerners but show western-like features in the Bantu, including an increased abundance of predictive carbohydrate and xenobiotic metabolic pathways. In contrast, the hunter-gatherer gut shows increased abundance of predicted virulence, amino acid, and vitamin metabolism functions, as well as dominance of lipid and amino-acid-derived metabolites, as determined through metabolomics. Our results demonstrate gradients of traditional subsistence patterns in two neighboring African groups and highlight the adaptability of the microbiome in response to host ecology.

BaAka women's health and subsistence practices in transitional conservation economies: Variation with age, household size, and food security.

OBJECTIVES: Using ethnographic interviews and biological measures, this article investigates changing health and nutrition of a hunter-gatherer population transitioning from a forest-based subsistence system to a horticultural and market-driven lifestyle. METHODS: This study represents biological and dietary recall data for adult female foragers (18+; n = 60) across two villages, Mossapoula (MS) and Yandoumbé (YDBE), in the Dzanga Sangha Protected Areas (APDS), Central African Republic (CAR). Standard anthropometric measurements (height, weight, skinfolds) and hemoglobin values were collected to assess short-term nutritional status. RESULTS: BMI was similar across all three age classes in YDBE, but differed amongst women of MS (ANOVA; F = 6.34, df = 30, P = 0.005).Values were lowest among the older women in older age class 3 who also had the greatest number of dependents. Overall SS values were significantly negatively correlated with the number of biological children (r = -0.33, P = 0.01) in both villages. CONCLUSIONS: Here, we identify older BaAka women, caring for their own children and grandchildren, as particularly vulnerable to economic changes and food insecurity. We found older women, especially those in a community with greater restrictions on access to forest resources to have more dependents, reduced market integration, and low BMI relative to younger women in the population. Am. J. Hum. Biol. 28:453-460, 2016. © 2015 Wiley Periodicals, Inc.

Examining short-term nutritional status among BaAka foragers in transitional economies.

Foragers in transitioning economies are at an increased risk of negative health outcomes as they undergo changes in subsistence patterns and diet. Here, we provide anthropometric data and examine the nutrition and health of adult BaAka foragers in relationship to declining wildlife and economic change in the Dzanga Sangha Protected Areas (APDS), Central African Republic. From June to August 2012, we collected biological data and dietary recall surveys from individuals in Mossapoula (MS) and Yandoumbé (YDBE) villages using standard anthropometric techniques and a single capillary blood finger prick. In our analysis, we identified variation in anthropometric measurements and hemoglobin levels by village (MS = 66, YDBE = 75) and gender (64 men, 77 women). Immigration, increased gun hunting and wildlife trades have reduced forager reliance on forest resources. These changes are evidenced in the marginal health of contemporary BaAka foragers of APDS. Although anthropometric measures of nutritional status do not significantly differ between communities, hemoglobin data highlight inequities in access to forest products between villages with different proximity to community hunting zones. Further, poor dietary diversity and low frequency of purchased foods in the diet indicate that the transition to a market economy has not been fully realized and diets are impoverished. Economic changes appear to have had the most impact at MS village, where forest use is most restricted and consumption of meat and forest products was reduced. This work highlights the nutritional and health needs of foragers in rapidly transitioning economies; especially those impacted by conservation management and zoning policies.

Reductions in primate abundance and diversity in a multiuse protected area: synergistic impacts of hunting and logging in a congo basin forest.

This article explores spatial and temporal changes in diurnal primate abundance and behavior in response to hunting, logging, and conservation at the Dzanga Sangha Dense Forest Reserve (RDS), Central African Republic over time. We use a combination of line-transect surveys in 2002 and 2009 (N = 540 km) and ethnographic interviews (N = 210) to investigate changes in the status of cercopithecines and colobines at RDS, with additional comparisons to earlier work. This protected area was lightly logged in the 1970s and the park was gazetted in 1990, with multiple-use reserve sectors allocated. Since the park's inception, hunting and the trade of primates have increased, along with human migration, greater accessibility of arms, and reduction of preferred ungulate prey. Primates have declined in both the park and reserve sectors. Our data further suggest that at RDS hunting has had a greater impact on primate diversity and abundance than logging. We have identified changes in species-specific vulnerability to hunting over time, with Cercopithecus nictitans and Lophocebus albigena initially having appeared to be relatively resistant to hunting pressure in 2002. However, subsequently as gun hunting has increased at RDS, these species have become vulnerable. Although monkeys at RDS have been responding behaviorally to increased gun hunting, they are not able to keep pace with changing hunting practices. This study allows us to begin to understand synergistic impacts of hunting and logging, necessary if we are to recommend strategies to better secure the future of primates in multiuse protected areas.