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      The role of exploitation in the establishment of mutualistic microbial symbioses

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          ABSTRACT

          Evolutionary theory suggests that the conditions required for the establishment of mutualistic symbioses through mutualism alone are highly restrictive, often requiring the evolution of complex stabilising mechanisms. Exploitation, whereby initially the host benefits at the expense of its symbiotic partner and mutual benefits evolve subsequently through trade-offs, offers an arguably simpler route to the establishment of mutualistic symbiosis. In this review, we discuss the theoretical and experimental evidence supporting a role for host exploitation in the establishment and evolution of mutualistic microbial symbioses, including data from both extant and experimentally evolved symbioses. We conclude that exploitation rather than mutualism may often explain the origin of mutualistic microbial symbioses.

          Abstract

          The authors review the theoretical and experimental evidence supporting exploitation as an alternative route to the evolution of mutualistic symbioses.

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          Most cited references63

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          The evolution of mutualisms: exploring the paths between conflict and cooperation.

          Mutualisms are of fundamental importance in all ecosystems but their very existence poses a series of challenging evolutionary questions. Recently, the application of molecular analyses combined with theoretical advances have transformed our understanding of many specific systems, thereby contributing to the possibility of a more general understanding of the factors that influence mutualisms.
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            Symbiotic bacterium modifies aphid body color.

            Color variation within populations of the pea aphid influences relative susceptibility to predators and parasites. We have discovered that infection with a facultative endosymbiont of the genus Rickettsiella changes the insects' body color from red to green in natural populations. Approximately 8% of pea aphids collected in Western Europe carried the Rickettsiella infection. The infection increased amounts of blue-green polycyclic quinones, whereas it had less of an effect on yellow-red carotenoid pigments. The effect of the endosymbiont on body color is expected to influence prey-predator interactions, as well as interactions with other endosymbionts.
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              Evolutionary transitions in bacterial symbiosis.

              Diverse bacterial lineages form beneficial infections with eukaryotic hosts. The origins, evolution, and breakdown of these mutualisms represent important evolutionary transitions. To examine these key events, we synthesize data from diverse interactions between bacteria and eukaryote hosts. Five evolutionary transitions are investigated, including the origins of bacterial associations with eukaryotes, the origins and subsequent stable maintenance of bacterial mutualism with hosts, the capture of beneficial symbionts via the evolution of strict vertical transmission within host lineages, and the evolutionary breakdown of bacterial mutualism. Each of these transitions has occurred many times in the history of bacterial-eukaryote symbiosis. We investigate these evolutionary events across the bacterial domain and also among a focal set of well studied bacterial mutualist lineages. Subsequently, we generate a framework for examining evolutionary transitions in bacterial symbiosis and test hypotheses about the selective, ecological, and genomic forces that shape these events.
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                Author and article information

                Journal
                FEMS Microbiol Lett
                FEMS Microbiol. Lett
                femsle
                FEMS Microbiology Letters
                Oxford University Press
                0378-1097
                1574-6968
                04 July 2019
                June 2019
                04 July 2019
                : 366
                : 12
                : fnz148
                Affiliations
                [1 ]Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
                [2 ]Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Cornwall TR10 9FE, UK
                [3 ]Department of Biology, University of York, York YO10 5DD, UK
                [4 ]Department of Mathematics, University of York, York YO10 5DD, UK
                Author notes
                Corresponding author: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK. Tel: +0114 222 0140; E-mail: messorensen1@ 123456sheffield.ac.uk
                Author information
                http://orcid.org/0000-0001-8983-2943
                http://orcid.org/0000-0003-0362-820X
                Article
                fnz148
                10.1093/femsle/fnz148
                6638607
                31271421
                4a849a6c-f350-4990-a5fa-94d5678b67f6
                © FEMS 2019.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 February 2019
                : 01 July 2019
                Page count
                Pages: 7
                Funding
                Funded by: Natural Environment Research Council 10.13039/501100000270
                Award ID: NE/K011774/2
                Funded by: Biotechnology and Biological Sciences Research Council 10.13039/501100000268
                Award ID: BB/M011151/1
                Categories
                Minireview
                Incubator - Microbial Symbioses
                Mini Review

                Microbiology & Virology
                microbiology,experimental evolution,microbial symbioses
                Microbiology & Virology
                microbiology, experimental evolution, microbial symbioses

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