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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.

 

Identifying patterns of pathogen infection in natural systems is crucial to understanding mechanisms of host–pathogen interactions. In this study, we explored how Junonia coenia densovirus (JcDV) infection varies over space and time in populations of the Melissa blue butterfly (Lycaeides melissa: Lycaenidae) using two different host plants. Collections ofL. melissaadults from multiple populations and years, along with host plant tissue and community samples of arthropods found on host plants, were screened to determine JcDV prevalence and load. Additionally, we sampled at multiple time points within a singleL. melissaflight season to investigate intra‐annual variation in infection patterns.

We found population‐specific variation in viral prevalence ofL. melissaacross collection years, with historical samples potentially having higher viral prevalence than contemporary samples, although host plant diet was not informative for these patterns. Patterns of infection across multiple generations within a flight season showed that late‐season samples had a higher proportion of JcDV‐positive individuals, suggesting an accumulation of virus over the season. Sequence data from a segment of the JcDV capsid gene showed a lack of viral genetic diversity betweenL. melissacollected from different localities, and little to no viral particles were found in the surrounding environment.

Our discovery of temporal variation in infection suggests that multiple sampling efforts must be made when describing pathogen prevalence in multivoltine hosts. Our findings represent an important first step towards further exploration of the ecological factors mediating disease prevalence and host‐specific variability of infection in wild insect populations.

 

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.

 

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. 

Background: Exotic plant species represent a novel resource for invertebrates and many herbivorous insects have incorporated exotic plants into their diet. Using a new host plant can have physiological repercussions for these herbivores that may be beneficial or detrimental. In this study, we compared how using an exotic versus native host plant affected the immune system response and feeding efficiency of a specialist lepidopteran, the common buckeye ( Junonia coenia : Nymphalidae, Hübner 1822). Materials and Methods: In a lab experiment, larvae were reared on either the exotic host plant, Plantago lanceolata (Plantaginaceae), or the native host plant, Mimulus guttatus (Phrymaceae). Beginning at second instar feeding efficiency data were collected every 2 days until fifth instar when immune assays were performed. Immune assays consisted of standing phenoloxidase activity, total phenoloxidase activity, and melanization. Results: Interestingly, we found that all three immune system parameters were higher on the exotic host plant compared to the native host plant. The exotic host plant also supported higher pupal weights, faster development time, greater consumption, and more efficient approximate digestibility. In contrast, the native host plant supported higher efficiency of conversion of ingested and digested food. The relationship between immunity and feeding efficiency was more complex but showed a large positive effect of greater host plant consumption on all immune parameters, particularly for the exotic host plant. While not as strong, the efficiency of conversion of digested food tended to show a negative effect on the three immune parameters. Conclusion: Overall, the exotic host plant proved to be beneficial for this specialist insect with regard to immunity and many of the feeding efficiency parameters and continued use of this host plant is predicted for populations already using it.