Dose relationships can exacerbate, mute, or reverse the impact of heterospecific host density on infection prevalence

Abstract

AbstractThe likelihood an individual becomes infected depends on the community in which it is embedded. For environmentally transmitted parasites, host community composition can alter host density, the density of parasites that hosts encounter in the environment, and the dose to which hosts are subsequently exposed. While some multi‐host theory incorporates some of these factors (e.g., competition among hosts), it does not currently consider the nonlinear relationships between parasite exposure dose and per‐propagule infectivity (dose–infectivity relationships), between exposure dose and infected host mortality (dose–mortality relationships), and between exposure dose and parasite propagule excretion (dose–excretion relationships). This makes it difficult to predict the impact of host species on one another’s likelihood of infection. To understand the implications of these nonlinear dose relationships for multi‐host communities, we first performed a meta‐analysis on published dose–infectivity experiments to quantify the proportion of accelerating, linear, or decelerating dose–infectivity relationships; we found that most experiments demonstrated decelerating dose–infectivity relationships. We then explored how dose–infectivity, dose–mortality, and dose–excretion relationships might alter the impact of heterospecific host density on infectious propagule density, infection prevalence, and density of a focal host using two‐host, one‐parasite models. We found that dose relationships either decreased the magnitude of the impact of heterospecific host density on propagule density and infection prevalence via negative feedback loops (decelerating dose–infectivity relationships, positive dose–mortality relationships, and negative dose–excretion relationships), or increased the magnitude of the impact of heterospecific host density on infection prevalence via positive feedback loops (accelerating dose–infectivity relationships and positive dose–excretion relationships). Further, positive dose–mortality relationships resulted in hosts that traditionally decrease disease (e.g., low competence, strong competitors) increasing infection prevalence, and vice versa. Finally, we found that dose relationships can create positive feedback loops that facilitate friendly competition (i.e., increased heterospecific density has a positive effect on focal host density because the reduction in disease outweighs the negative effects of interspecific competition). This suggests that without taking dose relationships into account, we may incorrectly predict the effect of heterospecific host interactions, and thus host community composition, on environmentally transmitted parasites.