Abstract
BackgroundIn host-parasite evolutionary arms races, parasites are generally expected to adapt more rapidly, due to their large population sizes and short generation times. There exist systems, though, where parasites cannot outpace their hosts because of similar generation times in both antagonists. In those cases concomitant adaptation is expected.MethodsWe tested this hypothesis in the three-spined stickleback-Schistocephalus solidus tapeworm system, where generation times are comparable in both organisms. We chose two populations of sticklebacks which differ prominently in the prevalence of S. solidus and consequently in its level of selective pressure. We performed a full factorial common garden experiment. Particularly, Norwegian (NO) and German (DE) sticklebacks, as well as hybrids between both stickleback populations and in both parental combinations, were exposed each to a single S. solidus originating from the same two host populations.ResultsWe found the infection phenotype to depend on the host population, the parasite population, but not their interaction. NO-parasites showed higher infectivity than DE-parasites, with NO-sticklebacks also being more resistant to DE-parasites than to the sympatric NO-parasite. Reciprocally, DE-hosts were more susceptible to the allopatric NO-parasite while DE-parasites grew less than NO-parasites in all stickleback groups. Despite this asymmetry, the ratio of worm to host weight, an indicator of parasite virulence, was identical in both sympatric combinations, suggesting an optimal virulence as a common outcome of parallel coevolved systems. In hybrid sticklebacks, intermediate infection rates and growth of S. solidus from either origin suggests a simple genetic basis of resistance. However, comparison of infection phenotypes in NO-maternal and DE-maternal hybrid sticklebacks indicates local adaptation to the sympatric counterpart in both the host and the parasite.ConclusionsHost-parasite systems with similar generation time show evidence for concomitant reciprocal adaptation resulting in parasite optimal virulence and host parasite specific resistance.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1419-3) contains supplementary material, which is available to authorized users.
Highlights
In host-parasite evolutionary arms races, parasites are generally expected to adapt more rapidly, due to their large population sizes and short generation times
The infection rates were of a similar order of magnitude, DE-parasites did not infect a laboratory strain of DE copepods obviously better than NO worms, as might be expected if there was adaptation to local copepod hosts
Out of 1200 sticklebacks, 69 fish died during the experiment and three exposed sticklebacks were found to be accidentally infected by two worms instead of one
Summary
In host-parasite evolutionary arms races, parasites are generally expected to adapt more rapidly, due to their large population sizes and short generation times. There exist systems, though, where parasites cannot outpace their hosts because of similar generation times in both antagonists. In those cases concomitant adaptation is expected. Hosts and parasites are engaged in an arms race where the evolution of traits associated with the interaction of both antagonists is the result of a mutually influenced trade-off between virulence and resistance. The conventional assumption is that parasites, due to their shorter generation time, larger population sizes and higher reproductive outputs, are ahead in this coevolutionary conflict and are more likely to locally adapt to their hosts [2,3,4]. While several studies found that parasites performed better in their sympatric hosts, others found hosts being better adapted to the local parasites than to allopatric conspecifics, and some studies found no effect at all
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