Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

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 either P. lanceolata or 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.

Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore

“…Plantago lanceolata produces two iridoid glycosides, aucubin and catalpol, that are sequestered by buckeye larvae, while M. guttatus does not produce these same iridoid glycosides. Prior data show that high levels of sequestration of these two iridoid glycosides reduces the immune response (Smilanich et al, 2009a;Carper et al, 2019;Muchoney et al, 2022); non-etheless, our data here show that individuals reared on P. lanceolata outperform individuals reared on M. guttatus, indicating that M. guttatus may be especially detrimental for immunity. While M. guttatus does not contain aucubin or catalpol, it does contain phenylpropanoid glycosides, specifically, verbascoside, which has been shown to be a feeding stimulant for J. coenia larvae but is not sequestered (Holeski et al, 2013).…”

“…While M. guttatus does not contain aucubin or catalpol, it does contain phenylpropanoid glycosides, specifically, verbascoside, which has been shown to be a feeding stimulant for J. coenia larvae but is not sequestered (Holeski et al, 2013). In a broader sense, the impact of novel host plants on herbivore immunity may provide insight into how new host plants become incorporated into the diet breadth of herbivores (Smilanich et al, 2018;Muchoney et al, 2022).…”

Use of an exotic host plant reduces viral burden in a native insect herbivore

“…As diet-mediated variation in development and immunity provided limited explanation, additional research will be necessary to elucidate how A. jatrophae reared on Plantago are able to suppress viral burdens and increase their likelihood of surviving infection. As the specific routes through which the immune response contributes to defence against JcDV are unclear (Muchoney et al, 2022;Resnik & Smilanich, 2020;Smilanich et al, 2018), it is possible that immune parameters that were not measured are enhanced in larvae consuming Plantago. In addition, the role of phytochemistry warrants consideration.…”

When does spatial clustering in caterpillars influence the relationship between population density and contact rates?

“…Stein et al 2011). Another interesting step would be to build spatially explicit individual based models of this system (Tardy et al, 2018) once we know more about the biology of JcDNV transmission, its effects on larval survival, and the possibility of shared reservoir hosts (e.g., Rivers and Longworth 1972;Mutuel et al, 2010;Muchoney et al 2022;Muchoney et al, 2023).…”

“…Adult females lay their eggs in batches, which suggests that more frequent interactions may occur among larval groups from adjacent oviposition locations. Finally, a densovirus (JcDNV) was recently found in E. phaeton populations in New England (Muchoney et al 2022). The disjunct nature of E. phaeton populations allows for an examination of the relationship between habitat use, population density, and con-speci c contact across independent populations.…”