Evolutionary Ecology of Multitrophic Interactions between Plants, Insect Herbivores and Entomopathogens

Abstract

Plants play an important role in the interactions between insect herbivores and their pathogens. Since the seminal review by Cory and Hoover (2006) on plant-mediated effects on insect-pathogen interactions, considerable progress has been made in understanding the complexity of these tritrophic interactions. Increasing interest in the areas of nutritional and ecological immunology over the last decade have revealed that plant primary and secondary metabolites can influence the outcomes of insect-pathogen interactions by altering insect immune functioning and physical barriers to pathogen entry. Some insects use plant secondary chemicals and nutrients to prevent infections (prophylactic medication) and medicate to limit the severity of infections (therapeutic medication). Recent findings suggest that there may be selectable plant traits that enhance entomopathogen efficacy, suggesting that entomopathogens could potentially impose selection pressure on plant traits that improve both pathogen and plant fitness. Moreover, plants in nature are inhabited by diverse communities of microbes, in addition to entomopathogens, some of which can trigger immune responses in insect herbivores. Plants are also shared by numerous other herbivorous arthropods with different modes of feeding that can trigger different defensive responses in plants. Some insect symbionts and gut microbes can degrade ingested defensive phytochemicals and be orally secreted onto wounded plant tissue during herbivory to alter plant defenses. Since non-entomopathogenic microbes and other arthropods are likely to influence the outcomes of plant-insect-entomopathogen interactions, I discuss a need to consider these multitrophic interactions within the greater web of species interactions.

Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds

“…Our results add to a substantial body of work that emphasises the role of environmental factors in phytophagous host–parasite interactions (Cory & Hoover ; Myers & Cory ; Shikano ). The largest declines in tolerance and increases in virulence occurred in monarchs feeding on A. curassavica , a species in which cardenolide production declined by nearly 25% when grown under eCO 2 .…”

“…Phytophagous insect-parasite systems are excellent models with which to study the indirect effects of global change on host-parasite interactions in the context of their communities. Host-plant quality mediates the impacts of parasites on phytophagous insects (Cory & Hoover 2006;Shikano 2017), with significant medicinal effects of plant secondary metabolites (Felton & Duffey 1990;Hunter & Schultz 1993;Bernays & Singer 2005). Importantly, plant nutritional and defensive chemistry vary in response to environmental change (Bidart-Bouzat & Imeh-Nathaniel 2008).…”

Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores’ Susceptibility to Natural Pathogens?

“…In a multitrophic context, the eventual outcome of the interaction between plant and herbivore is also modulated by pathogenic microbes, which is assumed to be due to direct as well as indirect effects of toxic phytochemicals on entomopathogen persistence and infectivity (19)(20)(21). Although some authors have speculated about the possibility of plants promoting the action or abundance of microbial entomopathogens (22), not much information is available about the impact of HIPVs on the pathogenicity of entomopathogens.…”

Phytochemical variation mediates the susceptibility of insect herbivores to entomoviruses

“…Entomoviruses play a key role in the relationships between plants and herbivorous insects. These tritrophic interactions are an increasingly important focus in chemical and evolutionary ecology (Cory & Hoover, ; Cory & Myers, ; Shikano, ). Among such tritrophic interactions, the bottom‐up effects of host plants on interactions between insects and their pathogenic viruses have been widely reported.…”