Nonlinear effects of temperature on mosquito parasite infection across a large geographic climate gradient

Temperature drives ectothermic host-parasite interactions, making them particularly sensitive to climatic variation and change. To isolate the role of temperature, lab-based studies are increasingly used to assess and forecast disease risk under current and future climate conditions. However, in the field, the effects of temperature on parasitism may be mediated by other sources of variation, including local adaptation of hosts and parasites to one another and to the environment. To address the key knowledge gaps of how temperature influences host-parasite interactions and whether thermal responses measured in controlled experiments capture infection across temperature gradients in nature, we paired an extensive field survey of parasitism-by the ciliate Lambornella clarki on its tree hole mosquito host, Aedes sierrensis-with laboratory experiments describing parasitism thermal performance curves (TPCs) for six host populations from varying climates. We also investigated the mechanisms underlying the thermal biology of the host-parasite interaction by separately measuring TPCs for infection, host immunity, and parasite growth rates. Along the west coast of North America, across an 1100-km climate gradient spanning 12°C mean rainy season temperature variation, we found that parasitism peaked at intermediately cold temperatures of 9.2-10°C and was consistent both between field seasons and with the lab experiment results. In the laboratory experiments, infection thermal responses were consistently nonlinear and peaked at 8.4-10°C, showing no evidence of host intraspecific variation in temperature sensitivity to parasitism. Importantly, parasitism peaked at temperatures below the thermal optimum for free-living L. clarki due to the balance of temperature effects on parasite growth and reproduction against the strength of the host melanization immune response. The results suggest that nonlinear responses to temperature drive parasitism in nature and that simple lab and field studies can accurately capture the thermal biology of multilayered host-parasite interactions.