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      The feedback between selection and demography shapes genomic diversity during coevolution

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          Abstract

          Rapid genomic changes during a coevolutionary arms race highlight the reciprocal effects of ecology and evolution.

          Abstract

          Species interactions and coevolution are integral to ecological communities, but we lack empirical information on when and how these interactions generate and purge genetic diversity. Using genomic time series data from host-virus experiments, we found that coevolution occurs through consecutive selective sweeps in both species, with temporal consistency across replicates. Sweeps were accompanied by phenotypic change (resistance or infectivity increases) and expansions in population size. In the host, population expansion enabled rapid generation of genetic diversity in accordance with neutral processes. Viral molecular evolution was, in contrast, confined to few genes, all putative targets of selection. This study demonstrates that molecular evolution during species interactions is shaped by both eco-evolutionary feedback dynamics and interspecific differences in how genetic diversity is generated and maintained.

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          Most cited references27

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          Biological and biomedical implications of the co-evolution of pathogens and their hosts.

          Co-evolution between host and pathogen is, in principle, a powerful determinant of the biology and genetics of infection and disease. Yet co-evolution has proven difficult to demonstrate rigorously in practice, and co-evolutionary thinking is only just beginning to inform medical or veterinary research in any meaningful way, even though it can have a major influence on how genetic variation in biomedically important traits is interpreted. Improving our understanding of the biomedical significance of co-evolution will require changing the way in which we look for it, complementing the phenomenological approach traditionally favored by evolutionary biologists with the exploitation of the extensive data becoming available on the molecular biology and molecular genetics of host-pathogen interactions.
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            Antagonistic coevolution accelerates molecular evolution.

            The Red Queen hypothesis proposes that coevolution of interacting species (such as hosts and parasites) should drive molecular evolution through continual natural selection for adaptation and counter-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity genes is consistent with this, the long time periods typically required to study coevolution have so far prevented any direct empirical test. Here we show, using experimental populations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage Phi2 (refs 10, 11), that the rate of molecular evolution in the phage was far higher when both bacterium and phage coevolved with each other than when phage evolved against a constant host genotype. Coevolution also resulted in far greater genetic divergence between replicate populations, which was correlated with the range of hosts that coevolved phage were able to infect. Consistent with this, the most rapidly evolving phage genes under coevolution were those involved in host infection. These results demonstrate, at both the genomic and phenotypic level, that antagonistic coevolution is a cause of rapid and divergent evolution, and is likely to be a major driver of evolutionary change within species.
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              WHEN IS IT COEVOLUTION?

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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                October 2019
                02 October 2019
                : 5
                : 10
                : eaax0530
                Affiliations
                [1 ]Department of Fish Ecology and Evolution, Center for Ecology, Evolution and Biogeochemistry, EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland.
                [2 ]Division of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.
                [3 ]Community Dynamics Group, Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Plön, Germany.
                [4 ]Group of Theoretical Biology, The State Key Laboratory of Biocontrol, School of Life Science, Sun Yat-sen University, Guangzhou, China.
                [5 ]Complex Systems and Networks Research Group, School of Mathematical Sciences, Queen Mary University of London, London, UK.
                [6 ]Evolutionary Genomics and Modelling Lab, Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK.
                [7 ]Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Plön, Germany.
                [8 ]Kiel Evolution Center, Biologiezentrum, Kiel, Germany.
                Author notes
                [*]

                These authors contributed equally to this work.

                [†]

                Present address: Ecology and Evolution Unit, Okinawa Institute of Science and Technology (OIST), Okinawa, Japan.

                [‡]

                These authors contributed equally to this work.

                [§]

                Present address: Limnological Institute University Konstanz, Aquatic Ecology and Evolution, Konstanz, Germany.

                [|| ]Corresponding author. Email: philine.feulner@ 123456eawag.ch
                Author information
                http://orcid.org/0000-0001-6677-0794
                http://orcid.org/0000-0003-1281-4987
                http://orcid.org/0000-0002-6857-8699
                http://orcid.org/0000-0002-3885-5253
                http://orcid.org/0000-0002-8078-1788
                Article
                aax0530
                10.1126/sciadv.aax0530
                6774728
                31616788
                3467d22a-481a-4481-ae62-ef0fbe61ff24
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

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

                History
                : 18 February 2019
                : 06 September 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 310030E-160812 / 1
                Funded by: German Research Foundation;
                Award ID: BE 4135/3-1, 4135/9
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Genetics
                Evolutionary Biology
                Custom metadata
                Nielsen Marquez

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