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      The Effects of Captivity on the Mammalian Gut Microbiome

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          Synopsis

          Recent studies increasingly note the effect of captivity or the built environment on the microbiome of humans and other animals. As symbiotic microbes are essential to many aspects of biology (e.g., digestive and immune functions), it is important to understand how lifestyle differences can impact the microbiome, and, consequently, the health of hosts. Animals living in captivity experience a range of changes that may influence the gut bacteria, such as diet changes, treatments, and reduced contact with other individuals, species and variable environmental substrates that act as sources of bacterial diversity. Thus far, initial results from previous studies point to a pattern of decreased bacterial diversity in captive animals. However, these studies are relatively limited in the scope of species that have been examined. Here we present a dataset that includes paired wild and captive samples from mammalian taxa across six Orders to investigate generalizable patterns of the effects captivity on mammalian gut bacteria. In comparing the wild to the captive condition, our results indicate that alpha diversity of the gut bacteria remains consistent in some mammalian hosts (bovids, giraffes, anteaters, and aardvarks), declines in the captive condition in some hosts (canids, primates, and equids), and increases in the captive condition in one host taxon (rhinoceros). Differences in gut bacterial beta diversity between the captive and wild state were observed for most of the taxa surveyed, except the even-toed ungulates (bovids and giraffes). Additionally, beta diversity variation was also strongly influenced by host taxonomic group, diet type, and gut fermentation physiology. Bacterial taxa that demonstrated larger shifts in relative abundance between the captive and wild states included members of the Firmicutes and Bacteroidetes. Overall, the patterns that we observe will inform a range of disciplines from veterinary practice to captive breeding efforts for biological conservation. Furthermore, bacterial taxa that persist in the captive state provide unique insight into symbiotic relationships with the host.

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          Most cited references18

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          Gut Microbiota and Extreme Longevity.

          The study of the extreme limits of human lifespan may allow a better understanding of how human beings can escape, delay, or survive the most frequent age-related causes of morbidity, a peculiarity shown by long-living individuals. Longevity is a complex trait in which genetics, environment, and stochasticity concur to determine the chance to reach 100 or more years of age [1]. Because of its impact on human metabolism and immunology, the gut microbiome has been proposed as a possible determinant of healthy aging [2, 3]. Indeed, the preservation of host-microbes homeostasis can counteract inflammaging [4], intestinal permeability [5], and decline in bone and cognitive health [6, 7]. Aiming at deepening our knowledge on the relationship between the gut microbiota and a long-living host, we provide for the first time the phylogenetic microbiota analysis of semi-supercentenarians, i.e., 105-109 years old, in comparison to adults, elderly, and centenarians, thus reconstructing the longest available human microbiota trajectory along aging. We highlighted the presence of a core microbiota of highly occurring, symbiotic bacterial taxa (mostly belonging to the dominant Ruminococcaceae, Lachnospiraceae, and Bacteroidaceae families), with a cumulative abundance decreasing along with age. Aging is characterized by an increasing abundance of subdominant species, as well as a rearrangement in their co-occurrence network. These features are maintained in longevity and extreme longevity, but peculiarities emerged, especially in semi-supercentenarians, describing changes that, even accommodating opportunistic and allochthonous bacteria, might possibly support health maintenance during aging, such as an enrichment and/or higher prevalence of health-associated groups (e.g., Akkermansia, Bifidobacterium, and Christensenellaceae).
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            Captivity humanizes the primate microbiome.

            The primate gastrointestinal tract is home to trillions of bacteria, whose composition is associated with numerous metabolic, autoimmune, and infectious human diseases. Although there is increasing evidence that modern and Westernized societies are associated with dramatic loss of natural human gut microbiome diversity, the causes and consequences of such loss are challenging to study. Here we use nonhuman primates (NHPs) as a model system for studying the effects of emigration and lifestyle disruption on the human gut microbiome. Using 16S rRNA gene sequencing in two model NHP species, we show that although different primate species have distinctive signature microbiota in the wild, in captivity they lose their native microbes and become colonized with Prevotella and Bacteroides, the dominant genera in the modern human gut microbiome. We confirm that captive individuals from eight other NHP species in a different zoo show the same pattern of convergence, and that semicaptive primates housed in a sanctuary represent an intermediate microbiome state between wild and captive. Using deep shotgun sequencing, chemical dietary analysis, and chloroplast relative abundance, we show that decreasing dietary fiber and plant content are associated with the captive primate microbiome. Finally, in a meta-analysis including published human data, we show that captivity has a parallel effect on the NHP gut microbiome to that of Westernization in humans. These results demonstrate that captivity and lifestyle disruption cause primates to lose native microbiota and converge along an axis toward the modern human microbiome.
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              Social networks predict gut microbiome composition in wild baboons

              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
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                Author and article information

                Journal
                Integr Comp Biol
                Integr. Comp. Biol
                icb
                Integrative and Comparative Biology
                Oxford University Press
                1540-7063
                1557-7023
                October 2017
                07 August 2017
                07 August 2017
                : 57
                : 4
                : 690-704
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, CO, USA
                [2 ]Department of Pediatrics and Computer Science & Engineering, University of California at San Diego, CA, USA
                [3 ]Institut des Sciences de l’Evolution, Université de Montpellier, UMR 5554, CNRS, IRD, EPHE, France
                [4 ]Department of Anthropology, Northwestern University, IL, USA
                [5 ]Department of Animal Sciences, Colorado State University, CO, USA
                [6 ]National Scientific and Technical Research Council (CONICET), Estacion Biologica Corrientes, Argentina
                [7 ]Department of Mammalogy, National Museum, Bloemfontein, South Africa
                [8 ]Centre for Environmental Management, University of the Free State, Bloemfontein, South Africa
                [9 ]Departamento de Ciencias Biologicas, Universidad de Los Andes, Bogotá, Colombia
                [10 ]Department of Anthropology, University of Texas Austin, TX, USA
                [11 ]Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Denmark
                [12 ]National High-Throughput DNA Sequencing Center, University of Copenhagen, Denmark
                [13 ]Association pour le cheval de Przewalski: TAKH, Station Biologique de la Tour du Valat, Arles 13200, France
                [14 ]Zoo Atlanta, GA, USA
                [15 ]School of Biological Sciences, Georgia Institute of Technology, GA, USA
                [16 ]Center for Microbiome Innovation, University of California at San Diego, La Jolla, CA, USA
                Author notes

                From the symposium “With a Little Help from My Friends: Microbial Partners in Integrative and Comparative Biology (SICB wide)” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2017 at New Orleans, Louisiana.

                Article
                icx090
                10.1093/icb/icx090
                5978021
                28985326
                1f9afd58-b3a7-40e7-9b44-b69b418e72a5
                © The Author 2017. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 15
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: IOS-1638630
                Categories
                With a Little Help from My Friends: Microbial Partners in Integrative and Comparative Biology (SICB wide)

                Comparative biology
                Comparative biology

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