Disease from leaves to landscapes: viral hotspots are determined by spatial arrangement and phytochemistry of host plants in specialist caterpillars

Although infectious diseases play a critical role in population regulation, our knowledge of complex drivers of disease for insects is limited. We conducted a field study on Baltimore checkerspot caterpillars (<i>Euphydryas phaeton</i>), chemical specialists on plants containing iridoid glycosides (IGs), to investigate the roles of host plant, phytochemistry, ontogeny and spatial associations in determining viral prevalence. We analysed individuals for viral presence and loads, quantified leaf IG concentrations from their native and novel host plants, and sequestered IGs in caterpillars. We found proximate caterpillar groups had greater similarity in infection prevalence, with areas of high prevalence indicating viral hotspots. Underlying variation in host plant chemistry corresponded to differences in viral prevalence. Furthermore, we used structural equation modeling to examine causal drivers of infection prevalence and loads. Advanced ontogeny was associated with increased viral prevalence and loads, as well as decreased sequestration of IGs. Infection loads were lower on the novel host plant, but prevalence was slightly higher, partially explained by decreased sequestration of IGs. Altogether, our findings reveal that spatial proximity, ontogeny, host plant species and secondary phytochemistry can all contribute to structuring infection risk, and thus offer insight into causal drivers of disease prevalence in complex plant-insect systems.