Alyssa N. Crittenden

Gut microbiome of the Hadza hunter-gatherers.

Human gut microbiota directly influences health and provides an extra means of adaptive potential to different lifestyles. To explore variation in gut microbiota and to understand how these bacteria may have co-evolved with humans, here we investigate the phylogenetic diversity and metabolite production of the gut microbiota from a community of human hunter-gatherers, the Hadza of Tanzania. We show that the Hadza have higher levels of microbial richness and biodiversity than Italian urban controls. Further comparisons with two rural farming African groups illustrate other features unique to Hadza that can be linked to a foraging lifestyle. These include absence of Bifidobacterium and differences in microbial composition between the sexes that probably reflect sexual division of labour. Furthermore, enrichment in Prevotella, Treponema and unclassified Bacteroidetes, as well as a peculiar arrangement of Clostridiales taxa, may enhance the Hadza’s ability to digest and extract valuable nutrition from fibrous plant foods.

A red meat-derived glycan promotes inflammation and cancer progression

Significance We present an unusual mechanism for the well-known association between red meat consumption and carcinoma risk involving the nonhuman sialic acid N-glycolylneuraminic acid (Neu5Gc). We first evaluate the Neu5Gc content of various foods to show that red meats are particularly rich in orally bioavailable Neu5Gc and then investigate human-like Neu5Gc-deficient mice fed this form of Neu5Gc. When such mice were challenged with anti-Neu5Gc antibodies, they developed evidence of systemic inflammation. Long-term exposure to this combination resulted in a significantly higher incidence of carcinomas (five-fold increase) and an association with Neu5Gc accumulation in the tumors. Similar mechanisms may contribute to the association of red meat consumption with other diseases, such as atherosclerosis and type 2 diabetes, which are also exacerbated by inflammation. A well known, epidemiologically reproducible risk factor for human carcinomas is the long-term consumption of “red meat” of mammalian origin. Although multiple theories have attempted to explain this human-specific association, none have been conclusively proven. We used an improved method to survey common foods for free and glycosidically bound forms of the nonhuman sialic acid N-glycolylneuraminic acid (Neu5Gc), showing that it is highly and selectively enriched in red meat. The bound form of Neu5Gc is bioavailable, undergoing metabolic incorporation into human tissues, despite being a foreign antigen. Interactions of this antigen with circulating anti-Neu5Gc antibodies could potentially incite inflammation. Indeed, when human-like Neu5Gc-deficient mice were fed bioavailable Neu5Gc and challenged with anti-Neu5Gc antibodies, they developed evidence of systemic inflammation. Such mice are already prone to develop occasional tumors of the liver, an organ that can incorporate dietary Neu5Gc. Neu5Gc-deficient mice immunized against Neu5Gc and fed bioavailable Neu5Gc developed a much higher incidence of hepatocellular carcinomas, with evidence of Neu5Gc accumulation. Taken together, our data provide an unusual mechanistic explanation for the epidemiological association between red meat consumption and carcinoma risk. This mechanism might also contribute to other chronic inflammatory processes epidemiologically associated with red meat consumption.

Metagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota

Through human microbiome sequencing, we can better understand how host evolutionary and ontogenetic history is reflected in the microbial function. However, there has been no information on the gut metagenome configuration in hunter-gatherer populations, posing a gap in our knowledge of gut microbiota (GM)-host mutualism arising from a lifestyle that describes over 90% of human evolutionary history. Here, we present the first metagenomic analysis of GM from Hadza hunter-gatherers of Tanzania, showing a unique enrichment in metabolic pathways that aligns with the dietary and environmental factors characteristic of their foraging lifestyle. We found that the Hadza GM is adapted for broad-spectrum carbohydrate metabolism, reflecting the complex polysaccharides in their diet. Furthermore, the Hadza GM is equipped for branched-chain amino acid degradation and aromatic amino acid biosynthesis. Resistome functionality demonstrates the existence of antibiotic resistance genes in a population with little antibiotic exposure, indicating the ubiquitous presence of environmentally derived resistances. Our results demonstrate how the functional specificity of the GM correlates with certain environment and lifestyle factors and how complexity from the exogenous environment can be balanced by endogenous homeostasis. The Hadza gut metagenome structure allows us to appreciate the co-adaptive functional role of the GM in complementing the human physiology, providing a better understanding of the versatility of human life and subsistence.

The Importance of Honey Consumption in Human Evolution

It has been suggested that honey may have been an important food source for early members of the genus Homo, yet the importance of meat and savanna plant foods continue to be stressed as the most relevant foods in dietary reconstructions. Here, the importance of honey and bee larvae in hominin diets is explored. Ethnographic reports, examples of Paleolithic rock art, and evidence from non-human primates are used to show that early hominins likely targeted beehives using the Oldowan tool kit. The consumption of honey and bee larvae likely provided significant amounts of energy, supplementing meat and plant foods. The ability to find and exploit beehives using stone tools may have been an innovation that allowed early Homo to nutritionally out-compete other species and may have provided critical energy to fuel the enlarging hominin brain.

Honey, Hadza, hunter-gatherers, and human evolution

Honey is the most energy dense food in nature. It is therefore not surprising that, where it exists, honey is an important food for almost all hunter-gatherers. Here we describe and analyze widespread honey collecting among foragers and show that where it is absent, in arctic and subarctic habitats, honey bees are also rare to absent. Second, we focus on one hunter-gatherer society, the Hadza of Tanzania. Hadza men and women both rank honey as their favorite food. Hadza acquire seven types of honey. Hadza women usually acquire honey that is close to the ground while men often climb tall baobab trees to raid the largest bee hives with stinging bees. Honey accounts for a substantial proportion of the kilocalories in the Hadza diet, especially that of Hadza men. Cross-cultural forager data reveal that in most hunter-gatherers, men acquire more honey than women but often, as with the Hadza, women do acquire some. Virtually all warm-climate foragers consume honey. Our closest living relatives, the great apes, take honey when they can. We suggest that honey has been part of the diet of our ancestors dating back to at least the earliest hominins. The earliest hominins, however, would have surely been less capable of acquiring as much honey as more recent, fully modern human hunter-gatherers. We discuss reasons for thinking our early ancestors would have acquired less honey than foragers ethnographically described, yet still significantly more than our great ape relatives.

Small-scale societies exhibit fundamental variation in the role of intentions in moral judgment

Significance It is widely considered a universal feature of human moral psychology that reasons for actions are taken into account in most moral judgments. However, most evidence for this moral intent hypothesis comes from large-scale industrialized societies. We used a standardized methodology to test the moral intent hypothesis across eight traditional small-scale societies (ranging from hunter-gatherer to pastoralist to horticulturalist) and two Western societies (one urban, one rural). The results show substantial variation in the degree to which an individual’s intentions influence moral judgments of his or her actions, with intentions in some cases playing no role at all. This dimension of cross-cultural variation in moral judgment may have important implications for understanding cultural disagreements over wrongdoing. Intent and mitigating circumstances play a central role in moral and legal assessments in large-scale industrialized societies. Although these features of moral assessment are widely assumed to be universal, to date, they have only been studied in a narrow range of societies. We show that there is substantial cross-cultural variation among eight traditional small-scale societies (ranging from hunter-gatherer to pastoralist to horticulturalist) and two Western societies (one urban, one rural) in the extent to which intent and mitigating circumstances influence moral judgments. Although participants in all societies took such factors into account to some degree, they did so to very different extents, varying in both the types of considerations taken into account and the types of violations to which such considerations were applied. The particular patterns of assessment characteristic of large-scale industrialized societies may thus reflect relatively recently culturally evolved norms rather than inherent features of human moral judgment.

Sex differences in Hadza eating frequency by food type

We investigate sex differences in frequencies of adults eating in a foraging population—the Hadza of Tanzania.

Hadza sleep biology: Evidence for flexible sleep‐wake patterns in hunter‐gatherers

OBJECTIVES Cross-cultural sleep research is critical to deciphering whether modern sleep expression is the product of recent selective pressures, or an example of evolutionary mismatch to ancestral sleep ecology. We worked with the Hadza, an equatorial, hunter-gatherer community in Tanzania, to better understand ancestral sleep patterns and to test hypotheses related to sleep segmentation. METHODS We used actigraphy to analyze sleep-wake patterns in thirty-three volunteers for a total of 393 days. Linear mixed effects modeling was performed to assess ecological predictors of sleep duration and quality. Additionally, functional linear modeling (FLM) was used to characterize 24-hr time averaged circadian patterns. RESULTS Compared with post-industrialized western populations, the Hadza were characterized by shorter (6.25 hr), poorer quality sleep (sleep efficiency = 68.9%), yet had stronger circadian rhythms. Sleep duration time was negatively influenced by greater activity, age, light (lux) exposure, and moon phase, and positively influenced by increased day length and mean nighttime temperature. The average daily nap ratio (i.e., the proportion of days where a nap was present) was 0.54 (SE = 0.05), with an average nap duration of 47.5 min (SE = 2.71; n = 139). DISCUSSION This study showed that circadian rhythms in small-scale foraging populations are more entrained to their ecological environments than Western populations. Additionally, Hadza sleep is characterized as flexible, with a consistent early morning sleep period yet reliance upon opportunistic daytime napping. We propose that plasticity in sleep-wake patterns has been a target of natural selection in human evolution.

Current views on hunter-gatherer nutrition and the evolution of the human diet

Diet composition and food choice are not only central to the daily lives of all living people, but are consistently linked with turning points in human evolutionary history. As such, scholars from a wide range of fields have taken great interest in the role that subsistence has played in both human cultural and biological evolution. Central to this discussion is the diet composition and nutrition of contemporary hunters and gatherers, who are frequently conscripted as model populations for ancestral human nutrition. Research among the worlds few remaining foraging populations is experiencing a resurgence, as they are making the final transition away from diets composed of wild foods, to those dominated by domesticated cultigens and/or processed foods. In an effort to glean as much information as possible, before such populations are no longer hunting and gathering, researchers interested in the evolution of human nutrition are rapidly collecting and accessing new and more data. Methods of scientific inquiry are in the midst of rapid change and scholars are able to revisit long-standing questions using state of the art analyses. Here, using the most relevant findings from studies in ethnography, nutrition, human physiology, and microbiomes, we provide a brief summary of the study of the evolution of human nutrition as it has specifically pertained to data coming from living hunter-gatherers. In doing so, we hope to bridge the disciplines that are currently invested in research on nutrition and health among foraging populations.

Fecal metabolome of the Hadza hunter-gatherers: A host-microbiome integrative view

The recent characterization of the gut microbiome of traditional rural and foraging societies allowed us to appreciate the essential co-adaptive role of the microbiome in complementing our physiology, opening up significant questions on how the microbiota changes that have occurred in industrialized urban populations may have altered the microbiota-host co-metabolic network, contributing to the growing list of Western diseases. Here, we applied a targeted metabolomics approach to profile the fecal metabolome of the Hadza of Tanzania, one of the world’s few remaining foraging populations, and compared them to the profiles of urban living Italians, as representative of people in the post-industrialized West. Data analysis shows that during the rainy season, when the diet is primarily plant-based, Hadza are characterized by a distinctive enrichment in hexoses, glycerophospholipids, sphingolipids, and acylcarnitines, while deplete in the most common natural amino acids and derivatives. Complementary to the documented unique metagenomic features of their gut microbiome, our findings on the Hadza metabolome lend support to the notion of an alternate microbiome configuration befitting of a nomadic forager lifestyle, which helps maintain metabolic homeostasis through an overall scarcity of inflammatory factors, which are instead highly represented in the Italian metabolome.