Advancing Theory Underlying Diversity-Disease Relationships: Competence in the Context of Life History, Demography, and Disease

Biodiversity loss can increase parasite transmission via the dilution effect when two criteria are met. First, if communities consist of hosts that span a gradient of competence, from highly competent species that amplify transmission to low-competence species that decrease transmission. Second, if biodiversity loss is non-random, such that low-diversity communities possess a disproportionately high number of highly competent hosts. Infection is then predicted to spread more efficiently in low-diversity (high competence) communities. These criteria offer a compelling direct connection between biodiversity loss and disease. Evaluating the processes underlying these criteria can provide insight into how commonly they are met, and when we can expect to observe parasite dilution. By pairing recently published competence values and high-resolution infection data from a multi-host multi-parasite system (five amphibian species and four trematode taxa), we evaluated core assumptions embedded in the dilution effect criteria: (1) Infection outcomes are governed by species competence; (2) community assembly is non-random; and (3) life history mediates an indirect connection between competence and community assembly. We found that competence was a strong predictor of infection in natural systems for the majority of host-parasite interactions. Community assembly order of amphibians was also predictable based on the spatiotemporal commonness of each species. While amphibian life history characteristics were associated with competence (with faster pace-of-life characteristics tied to higher levels of competence), we did not observe an association between life history characteristics and spatiotemporal patterns of commonness. Consequently, there was an idiosyncratic relationship between competence and assembly order. Simulations demonstrated that, even when the competence-assembly order relationship is absent, average community competence can still decline with species richness, as long as the most common species (first to assemble) has relatively high competence. By connecting life history, demography, competence, and infection, we found strong empirical support for some of the assumptions underlying the dilution effect; for those that were not met, we gained novel insight into the pathways through which community structure may lead to dilution.