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      A Microbial Perspective on the Grand Challenges in Comparative Animal Physiology

      research-article
      a ,
      mSystems
      American Society for Microbiology
      animal physiology, host-microbe interactions, organismal biology

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          Abstract

          Interactions with microbial communities can have profound influences on animal physiology, thereby impacting animal performance and fitness. Therefore, it is important to understand the diversity and nature of host-microbe interactions in various animal groups (invertebrates, fish, amphibians, reptiles, birds, and mammals).

          ABSTRACT

          Interactions with microbial communities can have profound influences on animal physiology, thereby impacting animal performance and fitness. Therefore, it is important to understand the diversity and nature of host-microbe interactions in various animal groups (invertebrates, fish, amphibians, reptiles, birds, and mammals). In this perspective, I discuss how the field of host-microbe interactions can be used to address topics that have been identified as grand challenges in comparative animal physiology: (i) horizontal integration of physiological processes across organisms, (ii) vertical integration of physiological processes across organizational levels within organisms, and (iii) temporal integration of physiological processes during evolutionary change. Addressing these challenges will require the use of a variety of animal models and the development of systems approaches that can integrate large, multiomic data sets from both microbial communities and animal hosts. Integrating host-microbe interactions into the established field of comparative physiology represents an exciting frontier for both fields.

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          Most cited references13

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          Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology.

          The accessibility of new genomic resources, high-throughput molecular technologies and analytical approaches such as genome scans have made finding genes contributing to fitness variation in natural populations an increasingly feasible task. Once candidate genes are identified, we argue that it is necessary to take a mechanistic approach and work up through the levels of biological organization to fully understand the impacts of genetic variation at these candidate genes. We demonstrate how this approach provides testable hypotheses about the causal links among levels of biological organization, and assists in designing relevant experiments to test the effects of genetic variation on phenotype, whole-organism performance capabilities and fitness. We review some of the research programs that have incorporated mechanistic approaches when examining naturally occurring genetic and phenotypic variation and use these examples to highlight the value of developing a comprehensive understanding of the relationship between genotype and fitness. We give suggestions to guide future research aimed at uncovering and understanding the genetic basis of adaptation and argue that further integration of mechanistic approaches will help molecular ecologists better understand the evolution of natural populations.
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            Divining the Essence of Symbiosis: Insights from the Squid-Vibrio Model

            Recent molecular data place microbes at the center of the biosphere, from ecosystem sustainability to animal and plant fitness. Models, including the squid-vibrio symbiosis described in this Essay, provide windows into underlying mechanisms that drive these systems.
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              Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores.

              For decades, ecologists have hypothesised that exposure to plant secondary compounds (PSCs) modifies herbivore-associated microbial community composition. This notion has not been critically evaluated in wild mammalian herbivores on evolutionary timescales. We investigated responses of the microbial communities of two woodrat species (Neotoma bryanti and N. lepida). For each species, we compared experienced populations that independently converged to feed on the same toxic plant (creosote bush, Larrea tridentata) to naïve populations with no exposure to creosote toxins. The addition of dietary PSCs significantly altered gut microbial community structure, and the response was dependent on previous experience. Microbial diversity and relative abundances of several dominant phyla increased in experienced woodrats in response to PSCs; however, opposite effects were observed in naïve woodrats. These differential responses were convergent in experienced populations of both species. We hypothesise that adaptation of the foregut microbiota to creosote PSCs in experienced woodrats drives this differential response.
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                Author and article information

                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                6 March 2018
                Mar-Apr 2018
                : 3
                : 2
                : e00146-17
                Affiliations
                [a ]Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
                Author notes
                Address correspondence to kevin.d.kohl@ 123456gmail.com .

                Conflict of Interest Disclosures: K.D.K. has nothing to disclose.

                Citation Kohl KD. 2018. A microbial perspective on the grand challenges in comparative animal physiology. mSystems 3:e00146-17. https://doi.org/10.1128/mSystems.00146-17.

                Article
                mSystems00146-17
                10.1128/mSystems.00146-17
                5853186
                29556549
                497ec6ee-d46d-4c19-a641-f36578ea51ef
                Copyright © 2018 Kohl.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 23 October 2017
                : 13 November 2017
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 19, Pages: 5, Words: 2728
                Categories
                Perspective
                Host-Microbe Biology
                Special Issue
                Custom metadata
                March/April 2018

                animal physiology,host-microbe interactions,organismal biology

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