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.
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.
We assessed the subsistence-related variation of the human gut microbiome at a fine resolution for two of the main dimensions of microbiome variation, age and geography. For this, we investigated the fecal microbiome and metabolome in rural Bassa and urbanized individuals from Nigeria, including infants, and compared data with worldwide populations practicing varying subsistence. Our data highlight specific microbiome traits that are progressively lost with urbanization, such as the dominance of pristine fiber degraders and the low inter-individual variation. For the Bassa, this last feature is the result of their subsistence-related practices favoring microbial dispersal, such as their extensive environmental contact and the usage of untreated waters from the Usuma River. The high degree of microbial dispersal observed in the Bassa meta-community nullifies the differences between infant and adult intestinal ecosystems, suggesting that the infant-type microbiome in Western populations could be the result of microbiome-associated neotenic traits favored by urbanization.
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 world's 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. K E Y W O R D Sdiet composition, forager, gut microbiome, human evolution, nutrition | I N T R O D U C T I O NDiet composition and food choice are indisputably a core facet in all human societies. Changes in diet are routinely associated with watershed moments in human evolution-such as tool making, brain expansion, family formation, cooperation, and even increased longevity (Aiello & Wheeler, 1995; Lee & DeVore, 1968;Wrangham, 2009). In the not-too-distant past, before industrialization, the rise of the middle class, and the development of market economies, procuring and preparing enough food to feed one's self and one's family occupied a significant portion of daily labor. In contemporary unindustrialized small-scale societies, this is still largely the case (Hawkes et al., 1997;Marlowe, 2010;Wood & Marlowe, 2013). Appropriately, anthropologists take great interest in the role that food and diet have had in human biological and cultural evolution (Messer, 1984). The old proverbs, "you are what you eat" and "tell me what you eat and I'll tell you what you are" (Brillat-Savarin, 1862) speak about food not only as a physical embodiment of the environment, but also as a means of social identity and symbolic construction of culture. Naturally, these are anthropological dialogues, but at their core, they speak the language of many fields of biology. In order for scholars interested in the evolution of the human diet to integrate work from various disciplines, a collective conversation ...
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.
Over the past decade, human microbiome research has energized the study of human evolution through a complete shift in our understanding of what it means to be human. The microbiome plays a pivotal role in human biology, performing key functions in digestion, mood and behavior, development and immunity, and a range of acute and chronic diseases. It is therefore critical to understand its evolution and changing ecology through time. Here we review recent findings on the microbiota of diverse human populations, non-human primates, and past human populations and discuss the implications of this research in formulating a deeper evolutionary understanding of the human holobiont.
Objectives: Paleofeces are valuable to archeologists and evolutionary biologists for their potential to yield health, dietary, and host information. As a rich source of preserved biomolecules from host-associated microorganisms, they can also provide insights into the recent evolution and changing ecology of the gut microbiome. However, there is currently no standard method for DNA extraction from paleofeces, which combine the dual challenges of complex biological composition and degraded DNA. Due to the scarcity and relatively poor preservation of paleofeces when compared with other archeological remains, it is important to use efficient methods that maximize ancient DNA (aDNA) recovery while also minimizing downstream taxonomic biases. Methods:In this study, we use shotgun metagenomics to systematically compare the performance of five DNA extraction methods on a set of well-preserved human and dog paleofeces from Mexico (~1,300 BP). Results:Our results show that all tested DNA extraction methods yield a consistent microbial taxonomic profile, but that methods optimized for ancient samples recover significantly more DNA.Conclusions: These results show promise for future studies that seek to explore the evolution of the human gut microbiome by comparing aDNA data with those generated in modern studies. K E Y W O R D S
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.
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