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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 (Euphydryas phaeton), 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. 

Abstract Pathogens play a key role in insect population dynamics, contributing to short‐term fluctuations in abundance as well as long‐term demographic trends. Two key factors that influence the effects of entomopathogens on herbivorous insect populations are modes of pathogen transmission and larval host plants. In this study, we examined tritrophic interactions between a sequestering specialist lepidopteran,Euphydryas phaeton, and a viral pathogen, Junonia coenia densovirus, on its native host plant,Chelone glabra, and a novel host plant,Plantago lanceolata, to explore whether host plant mediates viral transmission, survival, and viral loads. A two‐factor factorial experiment was conducted in the laboratory with natal larval clusters randomly assigned to either the native or novel host plant and crossed with either uninoculated controls or viral inoculation (20% of individuals in the cluster inoculated). Diapausing clusters were overwintered in the laboratory and checked weekly for mortality. At the end of diapause, all surviving individuals were reared to adulthood to estimate survivorship. All individuals were screened to quantify viral loads, and estimate horizontal transmission postmortem. To test for vertical transmission, adults were mated, and the progeny were screened for viral presence. Within virus‐treated groups, we found evidence for both horizontal and vertical transmission. Larval clusters reared on the native host plant had slightly higher horizontal transmission. Survival probability was lower in clusters feeding on the native host plant, with inoculated groups reared on the native host plant experiencing complete mortality. Viral loads did not differ by the host plant, although viral loads decreased with increased sequestration of secondary compounds on both host plants. Our results indicate that the use of a novel host plant may confer fitness benefits in terms of survival and reduced viral transmission when larvae feeding on it are infected with this pathogen, supporting hypotheses of potential evolutionary advantages of a host range expansion in the context of tritrophic interactions. 

Abstract Incorporation of exotic plants into the diets of native herbivores is a common phenomenon, influencing interactions with natural enemies and providing insight into the tritrophic costs and benefits of dietary expansion. We evaluated how use of an exotic plant, Plantago lanceolata , impacted immune performance, development and susceptibility to pathogen infection in the neotropical herbivore Anartia jatrophae (Lepidoptera: Nymphalidae). Caterpillars were reared on P. lanceolata or a native plant, Bacopa monnieri , and experimentally infected with a pathogenic virus, Junonia coenia densovirus. We found that virus‐challenged herbivores exhibited higher survival rates and lower viral burdens when reared on P. lanceolata compared to B. monnieri , though immune performance and development time were largely similar on the two plants. These findings reveal that use of an exotic plant can impact the vulnerability of a native herbivore to pathogen infection, suggesting diet‐mediated protection against disease as a potential mechanism facilitating the incorporation of novel resources. 

Abstract Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly,Euphydryas phaeton(Nymphalidae), have recently incorporated an exotic plant,Plantago lanceolata(Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus,Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using eitherP.lanceolataor a native plant,Chelone glabra(Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.