BackgroundIncreasing temperatures are predicted to strongly impact host-parasite interactions, but empirical tests are rare. Host species that are naturally exposed to a broad temperature spectrum offer the possibility to investigate the effects of elevated temperatures on hosts and parasites. Using three-spined sticklebacks, Gasterosteus aculeatus L., and tapeworms, Schistocephalus solidus (Müller, 1776), originating from a cold and a warm water site of a volcanic lake, we subjected sympatric and allopatric host-parasite combinations to cold and warm conditions in a fully crossed design. We predicted that warm temperatures would promote the development of the parasites, while the hosts might benefit from cooler temperatures. We further expected adaptations to the local temperature and mutual adaptations of local host-parasite pairs.ResultsOverall, S. solidus parasites grew faster at warm temperatures and stickleback hosts at cold temperatures. On a finer scale, we observed that parasites were able to exploit their hosts more efficiently at the parasite’s temperature of origin. In contrast, host tolerance towards parasite infection was higher when sticklebacks were infected with parasites at the parasite’s ‘foreign’ temperature. Cold-origin sticklebacks tended to grow faster and parasite infection induced a stronger immune response.ConclusionsOur results suggest that increasing environmental temperatures promote the parasite rather than the host and that host tolerance is dependent on the interaction between parasite infection and temperature. Sticklebacks might use tolerance mechanisms towards parasite infection in combination with their high plasticity towards temperature changes to cope with increasing parasite infection pressures and rising temperatures.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2192-7) contains supplementary material, which is available to authorized users.

Recent research provides accumulating evidence that the evolutionary dynamics of host-parasite adaptations strongly depend on environmental variation. In this context, the three-spined stickleback (Gasterosteus aculeatus) has become an important research model since it is distributed all over the northern hemisphere and lives in very different habitat types, ranging from marine to freshwater, were it is exposed to a huge diversity of parasites. While a majority of studies start from explorations of sticklebacks in the wild, only relatively few investigations have continued under laboratory conditions. Accordingly, it has often been described that sticklebacks differ in parasite burden between habitats, but the underlying co-evolutionary trajectories are often not well understood. With the present review, we give an overview of the most striking examples of stickleback-parasite-environment interactions discovered in the wild and discuss two model parasites which have received some attention in laboratory studies: the eye fluke Diplostomum pseudospathacaeum, for which host fish show habitat-specific levels of resistance, and the tapeworm Schistocephalus solidus, which manipulates immunity and behavior of its stickleback host to its advantage. Finally, we will concentrate on an important environmental variable, namely temperature, which has prominent effects on the activity of the immune system of ectothermic hosts and on parasite growth rates.

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It was suggested that parasite infections become more severe with rising temperature, as expected during global warming. In ectothermic systems, the growth of a parasite and therefore its reproductive capacity is expected to increase with temperature. However, the outcome of the interaction depends on the temperature optima of both host and parasite. Here we used experimental infections of three‐spined stickleback fish Gasterosteus aculeatus with its specific tapeworm parasite Schistocephalus solidus to investigate in detail the temperature optima for both host and parasite. We analyzed the fitness consequences thereof, focusing on growth and immunity of the host, and growth and offspring production of the parasite as fitness correlates. We checked for potential differences among populations, using the offspring of hosts and parasites derived from four study sites in Iceland, Germany and Spain that differ in average annual temperature ranging between 4.8°C and 18.4°C. We found differences in temperature optima of host and parasites that were quite consistent across the populations: while sticklebacks grew faster and had higher immune activity at low temperatures, the parasites did not even grow fast enough to reach sexual maturity in these conditions. By contrast, with increasing temperatures, parasite growth, egg production and offspring hatching increased strongly while host immunity and growth were impaired. Our results show that divergent temperature optima of hosts and parasites can have drastic fitness consequences and support the expectation that some parasites will benefit from global warming.