Individuals experience heterogeneous environmental conditions that can affect within-host processes such as immune defense against parasite infection. Variation among individuals in parasite shedding can cause some hosts to contribute disproportionately to population-level transmission, but we currently lack mechanistic theory that predicts when environmental conditions can result in large disease outbreaks through the formation of immunocompromised superspreading individuals. Here, I present a within-host model of a microparasite’s interaction with the immune system that links an individual host’s resource intake to its infectious period. For environmental scenarios driving population-level heterogeneity in resource intake (resource scarcity and resource subsidy relative to baseline availability), I generate a distribution of infectious periods and simulate epidemics on these heterogeneous populations. I find that resource scarcity can result in large epidemics through creation of superspreading individuals, while resource subsidies can reduce or prevent transmission of parasites close to their invasion threshold by homogenizing resource allocation to immune defense. Importantly, failure to account for heterogeneity in competence can result in under-prediction of outbreak size, especially when parasites are close to their invasion threshold. More generally, this framework suggests that differences in conditions experienced by individual hosts can lead to superspreading via differences in resource allocation to immune defense alone, even in the absence of other heterogeneites such as host contacts.
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Abstract Even though parasitic flatworms are one of the most species‐rich groups of hermaphroditic organisms, we know virtually nothing of their mating systems (selfing or kin‐mating rates) in nature. Hence, we lack an understanding of the role of inbreeding in parasite evolution. The natural mating systems of parasitic flatworms have remained elusive due to the inherent difficulty in generating progeny‐array data in many parasite systems. New developments in pedigree reconstruction allow direct inference of realized selfing rates in nature by simply using a sample of genotyped individuals. We built upon this advancement by utilizing the closed mating systems, that is, individual hosts, of endoparasites. In particular, we created a novel means to use pedigree reconstruction data to estimate potential kin‐mating rates. With data from natural populations of a tapeworm, we demonstrated how our newly developed methods can be used to test for cosibling transmission and inbreeding depression. We then showed how independent estimates of the two mating system components, selfing and kin‐mating rates, account for the observed levels of inbreeding in the populations. Thus, our results suggest that these natural parasite populations are in inbreeding equilibrium. Pedigree reconstruction analyses along with the new companion methods we developed will be broadly applicable across a myriad of parasite species. As such, we foresee that a new frontier will emerge wherein the diverse life histories of flatworm parasites could be utilized in comparative evolutionary studies to broadly address ecological factors or life history traits that drive mating systems and hence inbreeding in natural populations.
