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      Gut microbes limit growth in house sparrow nestlings ( Passer domesticus) but not through limitations in digestive capacity

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          Abstract

          Recent research often lauds the services and beneficial effects of host‐associated microbes on animals. However, hosting these microbes may come at a cost. For example, germ‐free and antibiotic‐treated birds generally grow faster than their conventional counterparts. In the wild, juvenile body size is correlated with survival, so hosting a microbiota may incur a fitness cost. Avian altricial nestlings represent an interesting study system in which to investigate these interactions, given that they exhibit the fastest growth rates among vertebrates, and growth is limited by their digestive capacity. We investigated whether reduction and restructuring of the microbiota by antibiotic treatment would: (i) increase growth and food conversion efficiency in nestling house sparrows ( Passer domesticus); (ii) alter aspects of gut anatomy or function (particularly activities of digestive carbohydrases and their regulation in response to dietary change); and (iii) whether there were correlations between relative abundances of microbial taxa, digestive function and nestling growth. Antibiotic treatment significantly increased growth and food conversion efficiency in nestlings. Antibiotics did not alter aspects of gut anatomy that we considered but depressed intestinal maltase activity. There were no significant correlations between abundances of microbial taxa and aspects of host physiology. Overall, we conclude that microbial‐induced growth limitation in developing birds is not driven by interactions with digestive capacity. Rather, decreased energetic and material costs of immune function or beneficial effects from microbes enriched under antibiotic treatment may underlie these effects. Understanding the costs and tradeoffs of hosting gut microbial communities represents an avenue of future research.

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          Most cited references46

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Antibiotic growth promoters in agriculture: history and mode of action

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              Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials.

              Three broiler feeding trials were investigated in order to identify gut bacteria consistently linked with improvements in bird performance as measured by feed efficiency. Trials were done in various geographic locations and varied in diet composition, broiler breed, and bird age. Gut microbial communities were investigated using microbial profiling. Eight common performance-linked operational taxonomic units (OTUs) were identified within both the ilea (180, 492, and 564-566) and ceca (140-142, 218-220, 284-286, 312, and 482) across trials. OTU 564-566 was associated with lower performance, while OTUs 140-142, 482, and 492 were associated with improved performance. Targeted cloning and sequencing of these eight OTUs revealed that they represented 26 bacterial species or phylotypes which clustered phylogenetically into seven groups related to Lactobacillus spp., Ruminococcaceae, Clostridiales, Gammaproteobacteria, Bacteroidales, Clostridiales/Lachnospiraceae, and unclassified bacteria/clostridia. Where bacteria were identifiable to the phylum level, they belonged predominantly to the Firmicutes, with Bacteroidetes and Proteobacteria also identified. Some of the potential performance-related phylotypes showed high sequence identity with classified bacteria (Lactobacillus salivarius, Lactobacillus aviarius, Lactobacillus crispatus, Faecalibacterium prausnitzii, Escherichia coli, Gallibacterium anatis, Clostridium lactatifermentans, Ruminococcus torques, Bacteroides vulgatus, and Alistipes finegoldii). The 16S rRNA gene sequence information generated will allow quantitative assays to be developed which will enable elucidations of which of these phylotypes are truly performance related. This information could be used to monitor strategies to improve feed efficiency and feed formulation for optimal gut health.
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                Author and article information

                Contributors
                kevin.d.kohl@gmail.com
                Journal
                Integr Zool
                Integr Zool
                10.1111/(ISSN)1749-4877
                INZ2
                Integrative Zoology
                John Wiley and Sons Inc. (Hoboken )
                1749-4869
                1749-4877
                14 March 2018
                March 2018
                : 13
                : 2 ( doiID: 10.1111/inz2.2018.13.issue-2 )
                : 139-151
                Affiliations
                [ 1 ] Department of Biological Sciences Vanderbilt University Nashville Tennessee USA
                [ 2 ] Department of Biological Sciences University of Pittsburgh Pittsburgh Pennsylvania USA
                [ 3 ] Department of Forest and Wildlife Ecology University of Wisconsin – Madison Madison Wisconsin USA
                [ 4 ] Department of Pathology, Microbiology, and Immunology Vanderbilt University Nashville Tennessee USA
                [ 5 ] Institute for Multidisciplinary Research in Biology of San Luis, National Scientific and Technical Research Council San Luis Argentina
                [ 6 ] Department of Biochemistry and Biological Sciences Universidad Nacional de San Luis San Luis Argentina
                Author notes
                [*] [* ] Correspondence: Kevin D. Kohl, University of Pittsburgh, 4249 Fifth Ave., Pittsburgh, PA 15260, USA. Email: kevin.d.kohl@ 123456gmail.com
                Article
                INZ212289
                10.1111/1749-4877.12289
                5873389
                29168619
                a2a087f7-0d2a-4bad-9f2e-97e08fc36794
                © 2017 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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                Page count
                Figures: 0, Tables: 0, References: 64, Pages: 13, Words: 2114
                Categories
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                Custom metadata
                2.0
                inz212289
                March 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.3.3 mode:remove_FC converted:28.03.2018

                antibiotics,food conversion efficiency,gut microbiota,host‐microbe interactions,maltase

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