When can we infer mechanism from parasite aggregation? A constraint-based approach to disease ecology

Few hosts have many parasites while many hosts have few parasites. This axiom of macroparasite aggregation is so pervasive it is considered a general law in disease ecology, with important implications for the dynamics of host-parasite systems. Because of these dynamical implications, a significant amount of work has explored both the various mechanisms leading to parasite aggregation patterns and how to infer mechanism from these patterns. However, as many disease mechanisms can produce similar aggregation patterns, it is not clear whether aggregation itself provides any additional information about mechanism. Here we apply a "constraint-based" approach developed in macroecology that allows us to explore whether parasite aggregation contains any additional information beyond what is provided by mean parasite load. We tested two constraint-based null models, both of which were constrained on the total number of parasites P and hosts H found in a sample, using data from 842 observed amphibian host-trematode parasite distributions. We found that constraint-based models captured ~85% of the observed variation in host-parasite distributions, suggesting that the constraints P and H contain much of the information about the shape of the host-parasite distribution. However, we also found that extending the constraint-based null models can identify the potential role of known aggregating mechanisms (such as host heterogeneity) and disaggregating mechanisms (such as parasite-induced host mortality) in constraining host-parasite distributions. Thus, by providing robust null models, constraint-based approaches can help guide investigations aimed at detecting biological processes that directly affect parasite aggregation above and beyond those that indirectly affect aggregation through P and H.