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      Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels ( Margaritifera margaritifera)

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          Abstract

          Host–parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long‐lived and highly host‐specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter‐lived host fish ( Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness‐related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts.

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          Arms races between and within species.

          An adaptation in one lineage (e.g. predators) may change the selection pressure on another lineage (e.g. prey), giving rise to a counter-adaptation. If this occurs reciprocally, an unstable runaway escalation or 'arms race' may result. We discuss various factors which might give one side an advantage in an arms race. For example, a lineage under strong selection may out-evolve a weakly selected one (' the life-dinner principle'). We then classify arms races in two independent ways. They may be symmetric or asymmetric, and they may be interspecific or intraspecific. Our example of an asymmetric interspecific arms race is that between brood parasites and their hosts. The arms race concept may help to reduce the mystery of why cuckoo hosts are so good at detecting cuckoo eggs, but so bad at detecting cuckoo nestlings. The evolutionary contest between queen and worker ants over relative parental investment is a good example of an intraspecific asymmetric arms race. Such cases raise special problems because the participants share the same gene pool. Interspecific symmetric arms races are unlikely to be important, because competitors tend to diverge rather than escalate competitive adaptations. Intraspecific symmetric arms races, exemplified by adaptations for male-male competition, may underlie Cope's Rule and even the extinction of lineages. Finally we consider ways in which arms races can end. One lineage may drive the other to extinction; one may reach an optimum, thereby preventing the other from doing so; a particularly interesting possibility, exemplified by flower-bee coevolution, is that both sides may reach a mutual local optimum; lastly, arms races may have no stable and but may cycle continuously. We do not wish necessarily to suggest that all, or even most, evolutionary change results from arms races, but we do suggest that the arms race concept may help to resolve three long-standing questions in evolutionary theory.
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            Virulence and local adaptation of a horizontally transmitted parasite.

            Parasites are thought to maximize the number of successfully transmitted offspring by trading off propagule production against host survival. In a horizontally transmitted microparasitic disease in Daphnia, a planktonic crustacean, increasing geographic distance between host and parasite origin was found to be correlated with a decrease in spore production and virulence. This finding indicates local adaptation of the parasite, but contradicts the hypothesis that long-standing coevolved parasites are less virulent than novel parasites. Virulence can be explained as the consequence of balancing the positive genetic correlation between host mortality and strain-specific spore production.
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              The effect of migration on local adaptation in a coevolving host-parasite system.

              Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites; that is, the greater infectivity of local parasites than foreign parasites on local hosts. Such parasite specialization on local hosts has implications for human health and agriculture. By contrast with classic single-species population-genetic models, theory indicates that parasite migration between subpopulations might increase parasite local adaptation, as long as migration does not completely homogenize populations. To test this hypothesis we developed a system-specific mathematical model and then coevolved replicate populations of the bacterium Pseudomonas fluorescens and a parasitic bacteriophage with parasite only, with host only or with no migration. Here we show that patterns of local adaptation have considerable temporal and spatial variation and that, in the absence of migration, parasites tend to be locally maladapted. However, in accord with our model, parasite migration results in parasite local adaptation, but host migration alone has no significant effect.
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                Author and article information

                Contributors
                janhavi.marwaha@uib.no
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                01 February 2017
                March 2017
                : 7
                : 5 ( doiID: 10.1002/ece3.2017.7.issue-5 )
                : 1375-1383
                Affiliations
                [ 1 ] Department of BiologyUniversity of Bergen BergenNorway
                [ 2 ] Aquatic Systems Biology UnitTechnical University of Munich FreisingGermany
                Author notes
                [*] [* ] Correspondence

                Janhavi Marwaha, Department of Biology, University of Bergen, Bergen, Norway.

                Email: janhavi.marwaha@ 123456uib.no

                Author information
                http://orcid.org/0000-0002-8644-642X
                Article
                ECE32740
                10.1002/ece3.2740
                5330927
                28261450
                67934874-50d1-414e-9899-c1a0aed6e133
                © 2017 The Authors. Ecology and Evolution 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
                : 10 May 2016
                : 17 December 2016
                Page count
                Figures: 5, Tables: 1, Pages: 9, Words: 7418
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32740
                March 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.0.7 mode:remove_FC converted:28.02.2017

                Evolutionary Biology
                coevolution,excystment,fitness,freshwater pearl mussel conservation,host–parasite system

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