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      Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

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          Abstract

          Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.

          Abstract

          In this study, we assessed the effects of environment, colony, and individual differences on abdominal bacterial communities in the ant Temnothorax nylanderi. Most interestingly, we discovered colony‐specific abdominal microbiomes in this ant, which suggests a role of host genetics, the social environment, or both in shaping the abdominal community. On top of that, we observed for the first time that colony microbial community diversity is positively correlated with productivity in a social insect.

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          Most cited references69

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          Symbiotic digestion of lignocellulose in termite guts.

          Their ability to degrade lignocellulose gives termites an important place in the carbon cycle. This ability relies on their partnership with a diverse community of bacterial, archaeal and eukaryotic gut symbionts, which break down the plant fibre and ferment the products to acetate and variable amounts of methane, with hydrogen as a central intermediate. In addition, termites rely on the biosynthetic capacities of their gut microbiota as a nutritional resource. The mineralization of humus components in the guts of soil-feeding species also contributes to nitrogen cycling in tropical soils. Lastly, the high efficiency of their minute intestinal bioreactors makes termites promising models for the industrial conversion of lignocellulose into microbial products and the production of biofuels.
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            A simple and distinctive microbiota associated with honey bees and bumble bees.

            Specialized relationships with bacteria often allow animals to exploit a new diet by providing a novel set of metabolic capabilities. Bees are a monophyletic group of Hymenoptera that transitioned to a completely herbivorous diet from the carnivorous diet of their wasp ancestors. Recent culture-independent studies suggest that a set of distinctive bacterial species inhabits the gut of the honey bee, Apis mellifera. Here we survey the gut microbiotae of diverse bee and wasp species to test whether acquisition of these bacteria was associated with the transition to herbivory in bees generally. We found that most bee species lack phylotypes that are the same or similar to those typical of A. mellifera, rejecting the hypothesis that this dietary transition was symbiont-dependent. The most common bacteria in solitary bee species are a widespread phylotype of Burkholderia and the pervasive insect associate, Wolbachia. In contrast, several social representatives of corbiculate bees do possess distinctive bacterial phylotypes. Samples of A. mellifera harboured the same microbiota as in previous surveys, and closely related bacterial phylotypes were identified in two Asian honey bees (Apis andreniformis and Apis dorsata) and several bumble bee (Bombus) species. Potentially, the sociality of Apis and Bombus species facilitates symbiont transmission and thus is key to the maintenance of a more consistent gut microbiota. Phylogenetic analyses provide a more refined taxonomic placement of the A. mellifera symbionts. © 2010 Blackwell Publishing Ltd.
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              Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont.

              Recent studies have shown that some plants and animals harbor microbial symbionts that protect them against natural enemies. Here we demonstrate that a maternally transmitted bacterium, Spiroplasma, protects Drosophila neotestacea against the sterilizing effects of a parasitic nematode, both in the laboratory and the field. This nematode parasitizes D. neotestacea at high frequencies in natural populations, and, until recently, almost all infections resulted in complete sterility. Several lines of evidence suggest that Spiroplasma is spreading in North American populations of D. neotestacea and that a major adaptive change to a symbiont-based mode of defense is under way. These findings demonstrate the profound and potentially rapid effects of defensive symbionts, which are increasingly recognized as major players in the ecology of species interactions.
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                Author and article information

                Contributors
                foitzik@uni-mainz.de
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                14 November 2019
                December 2019
                : 9
                : 23 ( doiID: 10.1002/ece3.v9.23 )
                : 13450-13467
                Affiliations
                [ 1 ] LOEWE Centre for Translational Biodiversity Genomics (LOEWE‐TBG) Frankfurt Germany
                [ 2 ] Behavioural Ecology and Social Evolution Institute of Organismic and Molecular Evolution Johannes Gutenberg University Mainz Germany
                [ 3 ] Evolutionary Ecology Institute of Organismic and Molecular Evolution Johannes Gutenberg University Mainz Germany
                [ 4 ]Present address: Applied Bioinformatics Group Institute of Cell Biology & Neuroscience Goethe University Frankfurt Germany
                Author notes
                [*] [* ] Correspondence

                Susanne Foitzik, Behavioural Ecology and Social Evolution, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Hanns Dieter Hüsch Weg 15, D‐55128 Mainz, Germany.

                Email: foitzik@ 123456uni-mainz.de

                Author information
                https://orcid.org/0000-0002-8149-3809
                https://orcid.org/0000-0001-9450-0345
                https://orcid.org/0000-0001-8161-6306
                Article
                ECE35801
                10.1002/ece3.5801
                6912891
                08bd9030-d722-419b-a3f0-ba4df4a8c679
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 August 2019
                : 30 September 2019
                : 03 October 2019
                Page count
                Figures: 10, Tables: 3, Pages: 18, Words: 14542
                Funding
                Funded by: Internal University Research Fund of the Johannes Gutenberg University
                Funded by: Hessen State Ministry of Higher Education, Research and the Arts , open-funder-registry 10.13039/501100003495;
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                December 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:16.12.2019

                Evolutionary Biology
                16s rrna sequencing,colony fitness,colony phenotype,gut bacteria,social insects,temnothorax

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