Beyond single host, single parasite interactions: quantifying competence for complete multi-host, multi-parasite communities

Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, "competence", is a critical currency for modeling transmission under community change and for testing diversity-disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.

We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi-host, multi-parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured twenty host-parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.

With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre-transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the twenty interactions was best explained by differences in barrier resistance and pre-transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.

We also produced dose-integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals, and doses was considerable, individual heterogeneity was limited compared to among-species differences. This finding highlights the robustness of our competence estimates and suggests that species-level values may be strong predictors for community-level transmission in natural systems.

Competence emerges from distinct underlying processes and can have strong species-level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns.