Amanda G. Henry

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.

Microfossils in calculus demonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium).

The nature and causes of the disappearance of Neanderthals and their apparent replacement by modern humans are subjects of considerable debate. Many researchers have proposed biologically or technologically mediated dietary differences between the two groups as one of the fundamental causes of Neanderthal disappearance. Some scenarios have focused on the apparent lack of plant foods in Neanderthal diets. Here we report direct evidence for Neanderthal consumption of a variety of plant foods, in the form of phytoliths and starch grains recovered from dental calculus of Neanderthal skeletons from Shanidar Cave, Iraq, and Spy Cave, Belgium. Some of the plants are typical of recent modern human diets, including date palms (Phoenix spp.), legumes, and grass seeds (Triticeae), whereas others are known to be edible but are not heavily used today. Many of the grass seed starches showed damage that is a distinctive marker of cooking. Our results indicate that in both warm eastern Mediterranean and cold northwestern European climates, and across their latitudinal range, Neanderthals made use of the diverse plant foods available in their local environment and transformed them into more easily digestible foodstuffs in part through cooking them, suggesting an overall sophistication in Neanderthal dietary regimes.

Mechanisms and causes of wear in tooth enamel: implications for hominin diets

The wear of teeth is a major factor limiting mammalian lifespans in the wild. One method of describing worn surfaces, dental microwear texture analysis, has proved powerful for reconstructing the diets of extinct vertebrates, but has yielded unexpected results in early hominins. In particular, although australopiths exhibit derived craniodental features interpreted as adaptations for eating hard foods, most do not exhibit microwear signals indicative of this diet. However, no experiments have yet demonstrated the fundamental mechanisms and causes of this wear. Here, we report nanowear experiments where individual dust particles, phytoliths and enamel chips were slid across a flat enamel surface. Microwear features produced were influenced strongly by interacting mechanical properties and particle geometry. Quartz dust was a rigid abrasive, capable of fracturing and removing enamel pieces. By contrast, phytoliths and enamel chips deformed during sliding, forming U-shaped grooves or flat troughs in enamel, without tissue loss. Other plant tissues seem too soft to mark enamel, acting as particle transporters. We conclude that dust has overwhelming importance as a wear agent and that dietary signals preserved in dental microwear are indirect. Nanowear studies should resolve controversies over adaptive trends in mammals like enamel thickening or hypsodonty that delay functional dental loss.

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.

Plant foods and the dietary ecology of Neanderthals and early modern humans

One of the most important challenges in anthropology is understanding the disappearance of Neanderthals. Previous research suggests that Neanderthals had a narrower diet than early modern humans, in part because they lacked various social and technological advances that lead to greater dietary variety, such as a sexual division of labor and the use of complex projectile weapons. The wider diet of early modern humans would have provided more calories and nutrients, increasing fertility, decreasing mortality and supporting large population sizes, allowing them to out-compete Neanderthals. However, this model for Neanderthal dietary behavior is based on analysis of animal remains, stable isotopes, and other methods that provide evidence only of animal food in the diet. This model does not take into account the potential role of plant food. Here we present results from the first broad comparison of plant foods in the diets of Neanderthals and early modern humans from several populations in Europe, the Near East, and Africa. Our data comes from the analysis of plant microremains (starch grains and phytoliths) in dental calculus and on stone tools. Our results suggest that both species consumed a similarly wide array of plant foods, including foods that are often considered low-ranked, like underground storage organs and grass seeds. Plants were consumed across the entire range of individuals and sites we examined, and none of the expected predictors of variation (species, geographic region, or associated stone tool technology) had a strong influence on the number of plant species consumed. Our data suggest that Neanderthal dietary ecology was more complex than previously thought. This implies that the relationship between Neanderthal technology, social behavior, and food acquisition strategies must be better explored.

The diet of Australopithecus sediba

Specimens of Australopithecus sediba from the site of Malapa, South Africa (dating from approximately 2 million years (Myr) ago) present a mix of primitive and derived traits that align the taxon with other Australopithecus species and with early Homo. Although much of the available cranial and postcranial material of Au. sediba has been described, its feeding ecology has not been investigated. Here we present results from the first extraction of plant phytoliths from dental calculus of an early hominin. We also consider stable carbon isotope and dental microwear texture data for Au. sediba in light of new palaeoenvironmental evidence. The two individuals examined consumed an almost exclusive C3 diet that probably included harder foods, and both dicotyledons (for example, tree leaves, fruits, wood and bark) and monocotyledons (for example, grasses and sedges). Like Ardipithecus ramidus (approximately 4.4 Myr ago) and modern savanna chimpanzees, Au. sediba consumed C3 foods in preference to widely available C4 resources. The inferred consumption of C3 monocotyledons, and wood or bark, increases the known variety of early hominin foods. The overall dietary pattern of these two individuals contrasts with available data for other hominins in the region and elsewhere.

The Role of Dust, Grit and Phytoliths in Tooth Wear

The threat of wear to dental enamel from hard particles of silica or silicates may have exerted great selective pressure on mammals. Increasing the hardness of enamel helps to forestall this, but capacity for variation is small because the tissue is almost entirely composed of hydroxyapatite. Hard though it is, enamel also displays considerable toughness, which is important in setting the sharpness of particles (defined as an attack angle) necessary to wear it. Added to the threat from environmental silica(tes) are phytoliths, particles of opaline silica embedded in plant tissues. We show here that phytoliths have very different properties to grit and dust and are unlikely to wear enamel. However, phytoliths would tend to fracture between teeth under similar conditions, so resembling natural agents of wear. In this context, we suggest that phytoliths could represent an example of mimicry, forming an example of a feeding deterrent operating by deceit.

To meat or not to meat? New perspectives on Neanderthal ecology.

Neanderthals have been commonly depicted as top predators who met their nutritional needs by focusing entirely on meat. This information mostly derives from faunal assemblage analyses and stable isotope studies: methods that tend to underestimate plant consumption and overestimate the intake of animal proteins. Several studies in fact demonstrate that there is a physiological limit to the amount of animal proteins that can be consumed: exceeding these values causes protein toxicity that can be particularly dangerous to pregnant women and newborns. Consequently, to avoid food poisoning from meat-based diets, Neanderthals must have incorporated alternative food sources in their daily diets, including plant materials as well.

Assessing Digestibility of Hadza Tubers Using a Dynamic In-Vitro Model

OBJECTIVES Bioaccessibility is a useful measure for assessing the biological value of a particular nutrient from food, especially foods such as tubers. The wild tubers exploited by Hadza foragers in Tanzania are of interest because they are nontoxic, consumed raw or briefly roasted, and entail substantial physical barriers to consumers. In this study, we attempted to elucidate the biological value of Hadza tubers by measuring the absorption of glucose through in-vitro digestion. METHODS We quantified digestibility using data from 24 experimental trials on four species of Hadza tuber using a dynamic in-vitro model that replicates digestion in the stomach and small intestine. Analysis of glucose in the input meal and output dialysate revealed the accessible glucose fraction. We also conducted assays for protein, vitamin, and mineral content on whole tubers and meal fractions. RESULTS Bioaccessibility of glucose varies depending on tuber species. Holding effects of chewing constant, brief roasting had negligible effects, but high intraspecific variation precludes interpretive power. Overall, Hadza tubers are very resistant to digestion, with between one- and two-thirds of glucose absorbed on average. Glucose absorption negatively correlated with glucose concentration of the tubers. CONCLUSIONS Roasting may provide other benefits such as ease of peeling and chewing to extract edible parenchymatous tissue. A powerful factor in glucose acquisition is tuber quality, placing emphasis on the skill of the forager. Other nutrient assays yielded unexpectedly high values for protein, iron, and iodine, making tubers potentially valuable resources beyond caloric content.

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.