The macroecology of immunity: predominant influence of climate on invertebrate immune response

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Abstract
The immune system is the primary defense against parasites. With the ever‐increasing rate of disease, epidemiologic models considering geographic variation in immune responses could prove useful. Despite increasing interest in the macroecology of parasitism and infectious diseases, we know little about the macroecology of immune responses (i.e. macroimmunology). Host characteristics, parasite exposure, and environmental factors can all affect immunity, but how these factors shape spatial variation in the strength of immune responses remains underexplored. We captured odonates (dragonflies and damselflies) and their conspicuous ectoparasitic mites from 42 sites spread across a geographic area spanning the temperate and boreal forest biomes in eastern Canada. We then conducted immune response bioassays on 1237 individuals from 63 odonate species. We used generalized additive models and structural equation models to relate immune responses to host body size, parasite load, pH, temperature and precipitation while accounting for spatial autocorrelation in immune ability and evolutionary relationships among host species. We found significant differences in the strength of immune response among host individuals, and this variation was best explained by climatic conditions, specifically strongly decreasing with precipitation. While host species significantly differed in immune response strength, we found no effect of host body size, evolutionary relationships among hosts, or parasitism on immune response. Our study investigating the drivers of immune response across dozens of species spread across two biomes is the most comprehensive to date. Climatic conditions have a strong influence on host immune response, regardless of host characteristics or parasitism rates. Strong immune responses were associated with low levels of annual precipitation, which could relate to the role of cuticular melanin content in desiccation resistance, and the melanin‐based encapsulation response being a byproduct of this adaptation. A spatially explicit understanding of the biological processes affecting immunity could improve epidemiological models of disease risk that inform disease management globally.
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