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      Social networks predict gut microbiome composition in wild baboons

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          Abstract

          Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations—a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.

          DOI: http://dx.doi.org/10.7554/eLife.05224.001

          eLife digest

          The digestive system is home to a complex community of microbes—known as the gut microbiome—that contributes to our health and wellbeing by digesting food, producing essential vitamins, and preventing the growth of harmful bacteria. The recent development of rapid genome sequencing techniques has made it much easier to identify the species of microbes found in the gut microbiome, and how this microbiome's composition varies between individuals.

          Studies in humans and other primates suggest that direct contact during social interactions may alter the composition of the gut microbiome in an individual. This could explain why there is a strong association between social interactions and health in humans and other social animals. However, similarities in the gut microbiomes of individuals within a social group could also be due to a shared diet or a common environment. The information collected during long-term studies of wild primates offers an opportunity to analyze and assess the influence of diet, environment and social interaction on the gut microbiome.

          Here, Tung et al. studied the gut microbiomes of 48 wild baboons belonging to two different social groups in Amboseli, Kenya. Using a technique called shotgun metagenomic sequencing, they sequenced DNA extracted from samples of feces collected from individual baboons. The sequence data revealed that an individual's social group and social network can predict the species found in its gut microbiome. This remained the case even when other factors—such as diet, kinship, and shared environments—were taken into account.

          Tung et al.'s findings suggest that direct physical contact during social interactions may be important in transmitting gut microbiomes between members of the same social group. However, scientists still don't know whether this exchange is good or bad for the health of the baboons. Future work will try to understand whether baboons benefit from acquiring gut microbes from their group members, and if the gut microbes of some social groups are better than others.

          DOI: http://dx.doi.org/10.7554/eLife.05224.002

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          Most cited references30

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          Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.

          E BERGMAN (1990)
          The VFA, also known as short-chain fatty acids, are produced in the gastrointestinal tract by microbial fermentation of carbohydrates and endogenous substrates, such as mucus. This can be of great advantage to the animal, since no digestive enzymes exist for breaking down cellulose or other complex carbohydrates. The VFA are produced in the largest amounts in herbivorous animal species and especially in the forestomach of ruminants. The VFA, however, also are produced in the lower digestive tract of humans and all animal species, and intestinal fermentation resembles that occurring in the rumen. The principal VFA in either the rumen or large intestine are acetate, propionate, and butyrate and are produced in a ratio varying from approximately 75:15:10 to 40:40:20. Absorption of VFA at their site of production is rapid, and large quantities are metabolized by the ruminal or large intestinal epithelium before reaching the portal blood. Most of the butyrate is converted to ketone bodies or CO2 by the epithelial cells, and nearly all of the remainder is removed by the liver. Propionate is similarly removed by the liver but is largely converted to glucose. Although species differences exist, acetate is used principally by peripheral tissues, especially fat and muscle. Considerable energy is obtained from VFA in herbivorous species, and far more research has been conducted on ruminants than on other species. Significant VFA, however, are now known to be produced in omnivorous species, such as pigs and humans. Current estimates are that VFA contribute approximately 70% to the caloric requirements of ruminants, such as sheep and cattle, approximately 10% for humans, and approximately 20-30% for several other omnivorous or herbivorous animals. The amount of fiber in the diet undoubtedly affects the amount of VFA produced, and thus the contribution of VFA to the energy needs of the body could become considerably greater as the dietary fiber increases. Pigs and some species of monkey most closely resemble humans, and current research should be directed toward examining the fermentation processes and VFA metabolism in those species. In addition to the energetic or nutritional contributions of VFA to the body, the VFA may indirectly influence cholesterol synthesis and even help regulate insulin or glucagon secretion. In addition, VFA production and absorption have a very significant effect on epithelial cell growth, blood flow, and the normal secretory and absorptive functions of the large intestine, cecum, and rumen. The absorption of VFA and sodium, for example, seem to be interdependent, and release of bicarbonate usually occurs during VFA absorption.(ABSTRACT TRUNCATED AT 400 WORDS)
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                2050-084X
                16 March 2015
                2015
                : 4
                : e05224
                Affiliations
                [1 ]deptDepartment of Evolutionary Anthropology , Duke University , Durham, United States
                [2 ]deptDepartment of Biology , Duke University , Durham, United States
                [3 ]deptInstitute of Primate Research , National Museums of Kenya , Nairobi, Kenya
                [4 ]deptDuke Population Research Institute , Duke University , Durham, United States
                [5 ]deptDepartment of Pediatrics, Sainte-Justine Hospital Research Centre , University of Montreal , Montreal, Canada
                [6 ]deptDepartment of Genetics, Cell Biology, and Development , University of Minnesota , Minneapolis, United States
                [7 ]deptDepartment of Ecology, Evolution, and Behavior , University of Minnesota , Minneapolis, United States
                [8 ]deptDepartment of Biological Sciences , University of Notre Dame , Notre Dame, United States
                [9 ]deptDepartment of Ecology and Evolutionary Biology , Princeton University , Princeton, United States
                MIT , United States
                MIT , United States
                Author notes
                [* ]For correspondence: jt5@ 123456duke.edu (JT);
                Article
                05224
                10.7554/eLife.05224
                4379495
                25774601
                5d1b4267-fdd7-4cf0-9faa-28cf776566d4
                © 2015, Tung et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 17 October 2014
                : 27 February 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: IOS 1053461
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: DEB 0919200
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000049, National Institute on Aging;
                Award ID: R01 AG034513
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000049, National Institute on Aging;
                Award ID: P01 AG031719
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Genomics and Evolutionary Biology
                Custom metadata
                2.3
                Social interactions can have a direct effect on the composition of the gut microbiome in wild primates.

                Life sciences
                papio cynocephalus,social behavior,gut microbiome,metagenomics,transmission,social network,other

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