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      Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch)

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          Abstract

          Vertebrates' diets profoundly influence the composition of symbiotic gut microbial communities. Studies documenting diet-microbiota associations typically focus on univariate or categorical diet variables. However, in nature individuals often consume diverse combinations of foods. If diet components act independently, each providing distinct microbial colonists or nutrients, we expect a positive relationship between diet diversity and microbial diversity. We tested this prediction within each of two fish species (stickleback and perch), in which individuals vary in their propensity to eat littoral or pelagic invertebrates or mixtures of both prey. Unexpectedly, in most cases individuals with more generalised diets had less diverse microbiota than dietary specialists, in both natural and laboratory populations. This negative association between diet diversity and microbial diversity was small but significant, and most apparent after accounting for complex interactions between sex, size and diet. Our results suggest that multiple diet components can interact non-additively to influence gut microbial diversity.

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          Most cited references34

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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
                Ecol Lett
                Ecol. Lett
                ele
                Ecology Letters
                BlackWell Publishing Ltd (Oxford, UK )
                1461-023X
                1461-0248
                August 2014
                22 May 2014
                : 17
                : 8
                : 979-987
                Affiliations
                [1 ]Howard Hughes Medical Institute and Section of Integrative Biology, University of Texas at Austin Austin, TX, 78712, USA
                [2 ]Section of Integrative Biology, University of Texas at Austin Austin, TX, 78712, USA
                [3 ]Program Man-Society-Environment, University of Basel Vesalgasse 1, Basel, CH-4051, Switzerland
                [4 ]Department of Ecology and Genetics, Uppsala University Norbyvägen 18D, Uppsala, SE-752 36, Sweden
                [5 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado Boulder, CO, 80309-0216, USA
                [6 ]Howard Hughes Medical Institute and Department of Chemistry and Biochemistry and BioFrontiers Institute, University of Colorado Boulder, CO, 80309-0215, USA
                [7 ]Department of Biological Sciences, Northern Arizona University Flagstaff, AZ, 86011, USA
                [8 ]Institute for Genomics and Systems Biology, Argonne National Laboratory Argonne, IL, 60439, USA
                Author notes
                *Correspondence: E-mail: danbolnick@ 123456austin.utexas.edu

                Editor, David Post

                Article
                10.1111/ele.12301
                4084827
                24847735
                2801ba1d-82f2-4676-ad1e-79921102118c
                © 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.

                This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 04 December 2013
                : 03 January 2014
                : 02 April 2014
                : 25 April 2014
                Categories
                Letters

                Ecology
                diet mixing,gasterosteus aculeatus,generalist,individual specialisation,microbiota,perca fluviatilis,perch,stable isotopes,threespine stickleback

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