Agricultural insect pests as models for studying stress-induced evolutionary processes.

Agricultural insect pests (AIPs) are widely successful in adapting to natural and anthropogenic stressors, repeatedly overcoming population bottlenecks and acquiring resistance to intensive management practices. Although they have been largely overlooked in evolutionary studies, AIPs are ideal systems for understanding rapid adaptation under novel environmental conditions. Researchers have identified several genomic mechanisms that likely contribute to adaptive stress responses, including positive selection on de novo mutations, polygenic selection on standing allelic variation and phenotypic plasticity (e.g., hormesis). However, new theory suggests that stress itself may induce epigenetic modifications, which may confer heritable physiological changes (i.e., stress-resistant phenotypes). In this perspective, we discuss how environmental stress from agricultural management generates the epigenetic and genetic modifications that are associated with rapid adaptation in AIPs. We summarise existing evidence for stress-induced evolutionary processes in the context of insecticide resistance. Ultimately, we propose that studying AIPs offers new opportunities and resources for advancing our knowledge of stress-induced evolution.

Rapid evolution of insecticide resistance in the Colorado potato beetle, Leptinotarsa decemlineata.

Despite considerable research, efforts to manage insecticide resistance continue to fail. The Colorado potato beetle (CPB), Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), epitomizes this problem, as it has repeatedly and rapidly evolved resistance to>50 insecticides. The patterns of resistance evolution are intriguing, as they defy models where resistance evolves from rare mutations. Here, we synthesize recent research on insecticide resistance in CPB showing that polygenic resistance drawn from standing genetic diversity explains genomic patterns of insecticide resistance evolution. However, rapid gene regulatory evolution suggests that other mechanisms might also facilitate adaptive change. We explore the hypothesis that sublethal stress from insecticide exposure could alter heritable epigenetic modifications, and discuss the range of experimental approaches needed to fully understand insecticide resistance evolution in this super pest.