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      When parasites disagree: Evidence for parasite-induced sabotage of host manipulation

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          Abstract

          Host manipulation is a common parasite strategy to alter host behavior in a manner to enhance parasite fitness usually by increasing the parasite's transmission to the next host. In nature, hosts often harbor multiple parasites with agreeing or conflicting interests over host manipulation. Natural selection might drive such parasites to cooperation, compromise, or sabotage. Sabotage would occur if one parasite suppresses the manipulation of another. Experimental studies on the effect of multi-parasite interactions on host manipulation are scarce, clear experimental evidence for sabotage is elusive. We tested the effect of multiple infections on host manipulation using laboratory-bred copepods experimentally infected with the trophically transmitted tapeworm Schistocephalus solidus. This parasite is known to manipulate its host depending on its own developmental stage. Coinfecting parasites with the same aim enhance each other's manipulation but only after reaching infectivity. If the coinfecting parasites disagree over host manipulation, the infective parasite wins this conflict: the noninfective one has no effect. The winning (i.e., infective) parasite suppresses the manipulation of its noninfective competitor. This presents conclusive experimental evidence for both cooperation in and sabotage of host manipulation and hence a proof of principal that one parasite can alter and even neutralize manipulation by another.

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          Most cited references55

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          Parasite Manipulation of Host Behavior

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            Innate defence: evidence for memory in invertebrate immunity.

            Acquired immunity in vertebrates is characterized by immunological memory and specificity, whereas the innate defence systems of invertebrates are assumed to have no specific memory. Here we use a model system of a copepod, which is a minute crustacean, and a parasitic tapeworm to show that the success of reinfection depends on the antigenic resemblance between the consecutively encountered parasites. This finding indicates that an invertebrate defence system may be capable of specific memory.
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              How and why Toxoplasma makes us crazy.

              For a long time, a latent toxoplasmosis, the lifelong presence of dormant stages of Toxoplasma in various tissues, including the brain, was considered harmless for immunocompetent persons. Within the past 10 years, however, many independent studies have shown that this parasitic disease, with a worldwide prevalence of about 30%, could be indirectly responsible for hundreds of thousands of deaths due to its effects on the rate of traffic and workplace accidents, and also suicides. Moreover, latent toxoplasmosis is probably one of the most important risk factors for schizophrenia. At least some of these effects, possibly mediated by increased dopamine and decreased tryptophan, are products of manipulation activity by Toxoplasma aiming to increase the probability of transmission from intermediate to definitive host through predation. Copyright © 2013. Published by Elsevier Ltd.
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                Author and article information

                Contributors
                Role: Associate Editor
                Role: Handling Editor
                Journal
                Evolution
                Evolution
                evo
                Evolution; International Journal of Organic Evolution
                Blackwell Publishing Ltd (Oxford, UK )
                0014-3820
                1558-5646
                March 2015
                10 March 2015
                : 69
                : 3
                : 611-620
                Affiliations
                [1 ]Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2 D-24306 Ploen, Germany
                Author notes
                Article
                10.1111/evo.12612
                4409835
                25643621
                61bfa79d-3fea-4133-9f5f-b6e9422e6478
                © 2015 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.

                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
                : 19 September 2014
                : 16 January 2015
                Categories
                Original Articles

                Evolutionary Biology
                cestode,conflict,cooperation,copepod,experimental infections,parasite–parasite interactions

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