Behavioral, Physiological, and Molecular Mechanisms Underlying the Adaptation of Helicoverpa armigera to the Fruits of a Marginal Host: Walnut (Juglans regia).

Abstract

In northwest China, changes in cultivation patterns and the scarcity of preferred hosts have forced Helicoverpa armigera to feed on the marginal host walnut (Juglans regia). However, the mechanisms allowing this adaptation remain poorly understood. Here, we investigated the behavioral, physiological, and molecular mechanisms underlying the local adaptation of this pest to walnut fruits. The green husk and shell generally contained higher levels of phytochemicals than the kernel. Bioassays revealed that the phytochemical-rich green husk and shell were less preferred, reduced larval fitness and growth, and elevated the activity of detoxification enzymes compared to the nutrient-rich kernel, which were further supported by a larger number of upregulated detoxification genes in insects fed green husks or shells based on transcriptome sequencing. Together, these data suggest that P450 genes (LOC110371778) may be crucial to H. armigera adaptation to the phytochemicals of walnuts. Our findings provide significant insight into the adaptation of H. armigera to walnut, an alternative host of lower quality. Meanwhile, our study provides a theoretical basis for managing resistance to H. armigera larvae in walnut trees and is instrumental in developing comprehensive integrated pest management strategies for this pest in walnut orchards and other agricultural systems.