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      Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

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          Abstract

          Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.

          Abstract

          Coinfections by multiple parasite species are a rule in nature and could affect host–parasite coevolutionary dynamics by altering infection dynamics. This simulation model shows that coinfections can enhance fluctuating selection dynamics between hosts and parasites when interactions between coinfecting species increase the fitness costs to the hosts. Under resource competition, however, coinfections can either enhance or suppress fluctuating selection dynamics.

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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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            Sex versus Non-Sex versus Parasite

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              Host-parasite 'Red Queen' dynamics archived in pond sediment.

              Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.
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                Author and article information

                Contributors
                otto.seppaelae@env.ethz.ch
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                30 August 2020
                September 2020
                : 10
                : 18 ( doiID: 10.1002/ece3.v10.18 )
                : 9600-9612
                Affiliations
                [ 1 ] Institute of Integrative Biology ETH Zürich Zürich Switzerland
                [ 2 ] Department of Aquatic Ecology Eawag Dübendorf Switzerland
                [ 3 ] Research Department for Limnology University of Innsbruck Mondsee Austria
                [ 4 ] Department of Biology Indiana University Bloomington IN USA
                Author notes
                [*] [* ] Correspondence

                Otto Seppälä, Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland.

                Email: otto.seppaelae@ 123456env.ethz.ch

                Author information
                https://orcid.org/0000-0001-7902-3069
                Article
                ECE36373
                10.1002/ece3.6373
                7520197
                1b676bf3-e209-4123-9404-e18469709f67
                © 2020 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
                : 11 February 2020
                : 15 April 2020
                : 22 April 2020
                Page count
                Figures: 5, Tables: 0, Pages: 13, Words: 8568
                Funding
                Funded by: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung , open-funder-registry 10.13039/501100001711;
                Award ID: 31003A 169531
                Funded by: Emil Aaltosen Säätiö , open-funder-registry 10.13039/501100004756;
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                September 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.1 mode:remove_FC converted:27.09.2020

                Evolutionary Biology
                coevolution,coinfection,red queen dynamics,resource competition,virulence
                Evolutionary Biology
                coevolution, coinfection, red queen dynamics, resource competition, virulence

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