Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk

Climate change may shift the timing and consequences of interspecific interactions, including those important to disease spread. Because hosts and pathogens may respond differentially to climate shifts, however, predicting the net effects on disease patterns remains challenging. Here, we used field data to guide a series of laboratory experiments that systematically evaluated the effects of temperature on the full infection process, including survival, penetration, establishment, persistence, and virulence of a highly pathogenic trematode (Ribeiroia ondatrae), and the development and survival of its amphibian host. Our results revealed nonlinearities in pathology as a function of temperature, which likely resulted from changes in both host and parasite processes. Both hosts and parasites responded strongly to temperature; hosts accelerated development while parasites showed enhanced host penetration but reduced establishment (encystment) and survival outside the host. While there were no differences in host survival among treatments, we observed a mid-temperature peak in parasite-induced deformities (63% at 20 degrees C), with the lowest frequency of deformities (12%) occurring at the highest temperature (26 degrees C). This nonlinear effect could result from temperature-driven changes in parasite burden owing to shifts in host penetration and/or clearance, reductions in host vulnerability owing to faster development, or both. Furthermore, despite strong temperature-driven changes in parasite penetration, survival, and establishment, the opposing nature of these effects lead to no difference in tadpole parasite burdens shortly after infection. These findings suggest that temperature-driven changes to the disease process may not be easily observable from comparison of parasite burdens alone, but multi-tiered experiments quantifying the responses of hosts, parasites and their interactions can enhance our ability to predict temperature-driven changes to disease risk. Climate-driven changes to disease patterns will therefore depend on underlying shifts in host and parasite development rates and the timing of their interactions.