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      Individual diet has sex-dependent effects on vertebrate gut microbiota

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          Abstract

          Vertebrates harbour diverse communities of symbiotic gut microbes. Host diet is known to alter microbiota composition, implying that dietary treatments might alleviate diseases arising from altered microbial composition (‘dysbiosis’). However, it remains unclear whether diet effects are general or depend on host genotype. Here we show that gut microbiota composition depends on interactions between host diet and sex within populations of wild and laboratory fish, laboratory mice and humans. Within each of two natural fish populations (threespine stickleback and Eurasian perch), among-individual diet variation is correlated with individual differences in gut microbiota. However, these diet–microbiota associations are sex dependent. We document similar sex-specific diet–microbiota correlations in humans. Experimental diet manipulations in laboratory stickleback and mice confirmed that diet affects microbiota differently in males versus females. The prevalence of such genotype by environment (sex by diet) interactions implies that therapies to treat dysbiosis might have sex-specific effects.

          Abstract

          Diet variations can alter gut microbial composition, but the potential influence of host genetic factors on these effects is unclear. Here, the authors show, in humans and in natural and laboratory fish populations, that such effects are dependent on the host’s sex, a genetically determined factor.

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          Most cited references35

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            The ecology of individuals: incidence and implications of individual specialization.

            Most empirical and theoretical studies of resource use and population dynamics treat conspecific individuals as ecologically equivalent. This simplification is only justified if interindividual niche variation is rare, weak, or has a trivial effect on ecological processes. This article reviews the incidence, degree, causes, and implications of individual-level niche variation to challenge these simplifications. Evidence for individual specialization is available for 93 species distributed across a broad range of taxonomic groups. Although few studies have quantified the degree to which individuals are specialized relative to their population, between-individual variation can sometimes comprise the majority of the population's niche width. The degree of individual specialization varies widely among species and among populations, reflecting a diverse array of physiological, behavioral, and ecological mechanisms that can generate intrapopulation variation. Finally, individual specialization has potentially important ecological, evolutionary, and conservation implications. Theory suggests that niche variation facilitates frequency-dependent interactions that can profoundly affect the population's stability, the amount of intraspecific competition, fitness-function shapes, and the population's capacity to diversify and speciate rapidly. Our collection of case studies suggests that individual specialization is a widespread but underappreciated phenomenon that poses many important but unanswered questions.
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              Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors.

              In vertebrates, including humans, individuals harbor gut microbial communities whose species composition and relative proportions of dominant microbial groups are tremendously varied. Although external and stochastic factors clearly contribute to the individuality of the microbiota, the fundamental principles dictating how environmental factors and host genetic factors combine to shape this complex ecosystem are largely unknown and require systematic study. Here we examined factors that affect microbiota composition in a large (n = 645) mouse advanced intercross line originating from a cross between C57BL/6J and an ICR-derived outbred line (HR). Quantitative pyrosequencing of the microbiota defined a core measurable microbiota (CMM) of 64 conserved taxonomic groups that varied quantitatively across most animals in the population. Although some of this variation can be explained by litter and cohort effects, individual host genotype had a measurable contribution. Testing of the CMM abundances for cosegregation with 530 fully informative SNP markers identified 18 host quantitative trait loci (QTL) that show significant or suggestive genome-wide linkage with relative abundances of specific microbial taxa. These QTL affect microbiota composition in three ways; some loci control individual microbial species, some control groups of related taxa, and some have putative pleiotropic effects on groups of distantly related organisms. These data provide clear evidence for the importance of host genetic control in shaping individual microbiome diversity in mammals, a key step toward understanding the factors that govern the assemblages of gut microbiota associated with complex diseases.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                29 July 2014
                : 5
                : 4500
                Affiliations
                [1 ]Howard Hughes Medical Institute and Department of Integrative Biology, University of Texas at Austin , One University Station C0990, Austin, Texas 78712, USA
                [2 ]Department of Integrative Biology, University of Texas at Austin , One University Station C0990, Austin, Texas 78712, USA
                [3 ]Department of Ecology and Genetics, Uppsala University , Norbyvägen 18D, SE-752 36 Uppsala, Sweden
                [4 ]Program Man-Society-Environment, University of Basel , Vesalgasse 1, CH-4051 Basel, Switzerland
                [5 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado , Boulder, Colorado 80309-0216, USA
                [6 ]Department of Medicine/Division of Cardiology, University of California , Los Angeles, California 90095-1675, USA
                [7 ]Howard Hughes Medical Institute and Department of Chemistry and Biochemistry and BioFrontiers Institute, University of Colorado , Boulder, Colorado 80309-0215, USA
                [8 ]Department of Biological Sciences, Northern Arizona University , Flagstaff, Arizona 86011, USA
                [9 ]Institute for Genomics and Systems Biology, Argonne National Laboratory , Argonne, Illinois 60439, USA
                Author notes
                Article
                ncomms5500
                10.1038/ncomms5500
                4279269
                25072318
                11e3a259-a183-480d-b6aa-0d170ff47b85
                Copyright © 2014, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 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-nc-sa/4.0/

                History
                : 03 December 2013
                : 25 June 2014
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