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.

Carl Woese Institute for Genomic Biology University of Illinois at Urbana Champaign Champaign Illinois USA

Central European Institute for Technology University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Department of Animal and Range Sciences Montana State University Bozeman Montana USA

Department of Animal Science University of Minnesota Twin Cities St Paul Minnesota USA

Department of Animal Sciences University of Illinois at Urbana Champaign Champaign Illinois USA

Department of Anthropology Dartmouth College Hanover New Hampshire USA

Department of Anthropology Hunter College of CUNY and New York Consortium in Evolutionary Primatology New York New York USA

Department of Anthropology Northwestern University Evanston Illinois USA

Department of Anthropology Purdue University West Lafayette Indiana USA

Department of Anthropology University of Colorado Boulder Colorado USA

Department of Anthropology University of Illinois at Urbana Champaign Champaign Illinois USA

Department of Anthropology University of Nevada Las Vegas Nevada USA

Department of Anthropology University of North Carolina Wilmington North Carolina USA

Department of Biology Loyola University Chicago Chicago Illinois USA

Department of Genetics Cell Biology and Development University of Minnesota Twin Cities Minneapolis Minnesota USA

Department of Microbiology University of Illinois at Urbana Champaign Champaign Illinois USA

Department of Nutrition and Exercise Physiology Elson S Floyd College of Medicine Washington State University Spokane Washington USA

Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Ceske Budejovice Czech Republic

Institute of Vertebrate Biology The Czech Academy of Sciences Brno Czech Republic

J Craig Venter Institute La Jolla California USA

Konrad Lorenz Institute for Evolution and Cognition Research Klosterneuburg Austria

Liberec Zoo Liberec Czech Republic

Metabolomics Center Roy J Carver Biotechnology Center University of Illinois at Urbana Champaign Champaign Illinois USA

World Wildlife Fund Dzanga Sangha Protected Areas Bayanga Central African Republic

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mSphere. 2021 Mar 17;6(2):e00168-21. doi: 10.1128/mSphere.00168-21. PubMed

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Interspecies variation in hominid gut microbiota controls host gene regulation

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