How priority effects within co-infected individuals scale up to affect disease risk in a two-host-two-pathogen system

An individual host’s risk of infection by a focal pathogen depends on the other host and pathogen species in the community. Using a model of two environmentally transmitted pathogens and two host species, we explore how priority effects within co-infected individuals and interspecific host competition jointly influence infection risk by a focal pathogen. To do this, we use infectious propagule density as a proxy for infection risk and compute explicit formulas for the (local) sensitivity of infectious propagule density of the focal pathogen to infectious propagule density of the alternative pathogen. We use the formulas to identify biological processes shaping the relationships between the infectious propagule densities, thus determining how infection risk by the focal pathogen changes as the abundance of the alternative pathogen increases. We find that the ranges of possible shapes of the relationships are predicted by the relative shedding and mortality rates of singly-infected and co-infected individuals of both species, but the host species with greater abundance and greater shedding rates has larger effects. We then simulate our model using parameter sets derived from Daphnia and their parasites and show how interspecific host competition and host susceptibility influence the shapes of the relationships. We find that asymmetric interspecific host competition reduces the range of possible shapes for the relationships because it suppresses the density of one host species whereas host susceptibility can increase the range of possible relationships. Our results show how within-host pathogen interactions can scale up to affect population-level measures of infection risk.