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      Bats Are an Untapped System for Understanding Microbiome Evolution in Mammals

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          Abstract

          Mammals evolved in a microbial world, and consequently, microbial symbionts have played a role in their evolution. An exciting new subdiscipline of metagenomics considers the ways in which microbes, particularly those found in the gut, have facilitated the ecological and phylogenetic radiation of mammals.

          ABSTRACT

          Mammals evolved in a microbial world, and consequently, microbial symbionts have played a role in their evolution. An exciting new subdiscipline of metagenomics considers the ways in which microbes, particularly those found in the gut, have facilitated the ecological and phylogenetic radiation of mammals. However, the vast majority of such studies focus on domestic animals, laboratory models, or charismatic megafauna (e.g., pandas and chimpanzees). The result is a plethora of studies covering few taxa across the mammal tree of life, leaving broad patterns of microbiome function and evolution unclear. Wildlife microbiome research urgently needs a model system in which to test hypotheses about metagenomic involvement in host ecology and evolution. We propose that bats (Order: Chiroptera) represent a model system ideal for comparative microbiome research, affording opportunities to examine host phylogeny, diet, and other natural history characteristics in relation to the evolution of the gut microbiome.

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          The delayed rise of present-day mammals.

          Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.
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            The microbiome and innate immunity.

            The intestinal microbiome is a signalling hub that integrates environmental inputs, such as diet, with genetic and immune signals to affect the host's metabolism, immunity and response to infection. The haematopoietic and non-haematopoietic cells of the innate immune system are located strategically at the host-microbiome interface. These cells have the ability to sense microorganisms or their metabolic products and to translate the signals into host physiological responses and the regulation of microbial ecology. Aberrations in the communication between the innate immune system and the gut microbiota might contribute to complex diseases.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSphere
                mSphere
                msph
                msph
                mSphere
                mSphere
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5042
                19 September 2018
                Sep-Oct 2018
                : 3
                : 5
                : e00397-18
                Affiliations
                [a ]Richard Gilder Graduate School, American Museum of Natural History, New York, New York, USA
                [b ]Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, New York, USA
                [c ]Division of Invertebrate Zoology, American Museum of Natural History, New York, New York, USA
                [d ]Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, USA
                University of Wisconsin—Madison
                Author notes
                Address correspondence to Melissa R. Ingala, ingala.melissar@ 123456gmail.com .

                Citation Ingala MR, Simmons NB, Perkins SL. 2018. Bats are an untapped system for understanding microbiome evolution in mammals. mSphere 3:e00397-18. https://doi.org/10.1128/mSphere.00397-18.

                Author information
                https://orcid.org/0000-0002-9866-5646
                Article
                mSphere00397-18
                10.1128/mSphere.00397-18
                6147128
                30232167
                f5bae343-25ed-40d7-b510-b33ef6dfe178
                Copyright © 2018 Ingala et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 63, Pages: 6, Words: 4460
                Funding
                Funded by: American Museum of Natural History (AMNH), https://doi.org/10.13039/100005835;
                Award Recipient :
                Categories
                Perspective
                Host-Microbe Biology
                Custom metadata
                September/October 2018

                chiroptera,bats,macroevolution,microbial ecology,microbiota
                chiroptera, bats, macroevolution, microbial ecology, microbiota

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