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      Unraveling the processes shaping mammalian gut microbiomes over evolutionary time

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          Abstract

          Whether mammal–microbiome interactions are persistent and specific over evolutionary time is controversial. Here we show that host phylogeny and major dietary shifts have affected the distribution of different gut bacterial lineages and did so on vastly different bacterial phylogenetic resolutions. Diet mostly influences the acquisition of ancient and large microbial lineages. Conversely, correlation with host phylogeny is mostly seen among more recently diverged bacterial lineages, consistent with processes operating at similar timescales to host evolution. Considering microbiomes at appropriate phylogenetic scales allows us to model their evolution along the mammalian tree and to infer ancient diets from the predicted microbiomes of mammalian ancestors. Phylogenetic analyses support co-speciation as having a significant role in the evolution of mammalian gut microbiome compositions. Highly co-speciating bacterial genera are also associated with immune diseases in humans, laying a path for future studies that probe these co-speciating bacteria for signs of co-evolution.

          Abstract

          Both host diet and phylogeny have been argued to shape mammalian microbiome communities. Here, the authors show that diet predicts the presence of ancient bacterial lineages in the microbiome, but that co-speciation between more recent bacterial lineages and their hosts may drive associations between microbiome composition and phylogeny.

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          Most cited references 38

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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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            NULL MODEL ANALYSIS OF SPECIES CO-OCCURRENCE PATTERNS

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              Cospeciation of gut microbiota with hominids.

              The evolutionary origins of the bacterial lineages that populate the human gut are unknown. Here we show that multiple lineages of the predominant bacterial taxa in the gut arose via cospeciation with humans, chimpanzees, bonobos, and gorillas over the past 15 million years. Analyses of strain-level bacterial diversity within hominid gut microbiomes revealed that clades of Bacteroidaceae and Bifidobacteriaceae have been maintained exclusively within host lineages across hundreds of thousands of host generations. Divergence times of these cospeciating gut bacteria are congruent with those of hominids, indicating that nuclear, mitochondrial, and gut bacterial genomes diversified in concert during hominid evolution. This study identifies human gut bacteria descended from ancient symbionts that speciated simultaneously with humans and the African apes.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                23 February 2017
                2017
                : 8
                Affiliations
                [1 ]Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology , Cambridge, Massachusetts 02139, USA
                [2 ]Department of Biological Engineering, Massachusetts Institute of Technology , Cambridge, Massachusetts 02139, USA
                [3 ]Laboratoire d Ecologie Alpine, CNRS, University of Grenoble Alpes, FR-38041 , Grenoble Cedex 9, France
                [4 ]Organismic and Evolutionary Biology, Harvard University , 26 Oxford St, Cambridge, Massachusetts 02138, USA
                [5 ]The Broad Institute of MIT and Harvard , 415 Main Street Cambridge, Massachusetts 02142, USA
                Author notes
                [*]

                These authors contributed equally to this work

                Article
                ncomms14319
                10.1038/ncomms14319
                5331214
                28230052
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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