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      Understanding the ecology and evolution of host–parasite interactions across scales

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          Abstract

          Predicting the emergence, spread and evolution of parasites within and among host populations requires insight to both the spatial and temporal scales of adaptation, including an understanding of within‐host up through community‐level dynamics. Although there are very few pathosystems for which such extensive data exist, there has been a recent push to integrate studies performed over multiple scales or to simultaneously test for dynamics occurring across scales. Drawing on examples from the literature, with primary emphasis on three diverse host–parasite case studies, we first examine current understanding of the spatial structure of host and parasite populations, including patterns of local adaptation and spatial variation in host resistance and parasite infectivity. We then explore the ways to measure temporal variation and dynamics in host–parasite interactions and discuss the need to examine change over both ecological and evolutionary timescales. Finally, we highlight new approaches and syntheses that allow for simultaneous analysis of dynamics across scales. We argue that there is great value in examining interplay among scales in studies of host–parasite interactions.

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          Most cited references65

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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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            Bacteria-phage antagonistic coevolution in soil.

            Bacteria and their viruses (phages) undergo rapid coevolution in test tubes, but the relevance to natural environments is unclear. By using a "mark-recapture" approach, we showed rapid coevolution of bacteria and phages in a soil community. Unlike coevolution in vitro, which is characterized by increases in infectivity and resistance through time (arms race dynamics), coevolution in soil resulted in hosts more resistant to their contemporary than past and future parasites (fluctuating selection dynamics). Fluctuating selection dynamics, which can potentially continue indefinitely, can be explained by fitness costs constraining the evolution of high levels of resistance in soil. These results suggest that rapid coevolution between bacteria and phage is likely to play a key role in structuring natural microbial communities.
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              Multiple infections and the evolution of virulence.

              Infections that consist of multiple parasite strains or species are common in the wild and are a major public health concern. Theory suggests that these infections have a key influence on the evolution of infectious diseases and, more specifically, on virulence evolution. However, we still lack an overall vision of the empirical support for these predictions. We argue that within-host interactions between parasites largely determine how virulence evolves and that experimental data support model predictions. Then, we explore the main limitation of the experimental study of such 'mixed infections', which is that it draws conclusions on evolutionary outcomes from studies conducted at the individual level. We also discuss differences between coinfections caused by different strains of the same species or by different species. Overall, we argue that it is possible to make sense out of the complexity inherent to multiple infections and that experimental evolution settings may provide the best opportunity to further our understanding of virulence evolution. © 2013 Blackwell Publishing Ltd/CNRS.
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                Author and article information

                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                20 August 2015
                January 2016
                : 9
                : 1 , Women's contribution to basic and applied evolutionary biology ( doiID: 10.1111/eva.2016.9.issue-1 )
                : 37-52
                Affiliations
                [ 1 ] Department of Biosciences Metapopulation Research CentreUniversity of Helsinki HelsinkiFinland
                [ 2 ] BiosciencesUniversity of Exeter TremoughUK
                [ 3 ] Integrative BiologyUniversity of California BerkeleyUSA
                Author notes
                [*] [* ] Correspondence

                Britt Koskella, Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

                Tel.: +1‐510‐6423281;

                fax: +1‐510‐6436264;

                e‐mail: bkoskella@ 123456berkeley.edu

                Article
                EVA12294
                10.1111/eva.12294
                4780374
                27087838
                280685fc-697d-459a-b6f9-2a8a55925354
                © 2015 The Authors. Evolutionary Applications published by John Wiley & Sons 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.

                History
                : 02 April 2015
                : 18 June 2015
                Page count
                Pages: 16
                Funding
                Funded by: Academy of Finland
                Award ID: 284601
                Award ID: 136393
                Funded by: European Research Council
                Award ID: PATHEVOL 400820
                Funded by: UK Natural Environment Research Council
                Award ID: NE/K00879X/1
                Categories
                Review and Syntheses
                Review and Syntheses
                Custom metadata
                2.0
                eva12294
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.8.4 mode:remove_FC converted:07.03.2016

                Evolutionary Biology
                coevolution,eco‐evolutionary dynamics,host–parasite,local adaptation,parasite‐driven evolution,spatial structure,spatiotemporal,time shift

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