Is the local environment more important than within-host interactions in determining coinfection?

Abstract

Host populations often vary in the magnitude of coinfection they experience across environmental gradients. Furthermore, coinfection often occurs sequentially, with a second parasite infecting the host after the first has established a primary infection. Because the local environment and interactions between coinfecting parasites can both drive patterns of coinfection, it is important to disentangle the relative contributions of environmental factors and within-host interactions to patterns of coinfection. Here, we develop a conceptual framework and present an empirical case study to disentangle these facets of coinfection. Across multiple lakes, we surveyed populations of five damselfly (host) species and quantified primary parasitism by aquatic, ectoparasitic water mites and secondary parasitism by terrestrial, endoparasitic gregarines. We first asked if coinfection is predicted by abiotic and biotic factors within the local environment, finding that the probability of coinfection decreased for all host species as pH increased. We then asked if primary infection by aquatic water mites mediated the relationship between pH and secondary infection by terrestrial gregarines. Contrary to our expectations, we found no evidence for a water mite-mediated relationship between pH and gregarines. Instead, the intensity of gregarine infection correlated solely with the local environment, with the magnitude and direction of these relationships varying among environmental predictors. Our findings emphasize the role of the local environment in shaping infection dynamics that set the stage for coinfection. Although we did not detect within-host interactions, the approach herein can be applied to other systems to elucidate the nature of interactions between hosts and coinfecting parasites within complex ecological communities.