Transgenerational epigenetic inheritance of insecticide resistance in invasive Colorado potato beetles (Leptinotarsa decemlineata)

Some insect pests, such as the Colorado potato beetle Leptinotarsa decemlineata; CPB), are capable of rapidly evolving resistance to a wide range of chemical insecticides. While standing or de novo genetic variation likely play important roles in this process, genetics cannot fully explain why resistance phenotypes evolve rapidly and repeatedly in CPB. Another possible mechanism contributing to rapid adaptation may be inheritance of stress-induced epigenetic modification, e.g., genome-wide reduction in DNA methylation, and associated changes in gene expression.
We tested whether insecticide exposure influences transgenerational inheritance of DNA methylation and elevated insecticide tolerance. Across eight replicate mated-pair lineages, we exposed third instar CPB larvae (F₀ generation) to either an LC₂₅ dose of imidacloprid (treatment) or water (control). We reared lineages separately for three successive generations and measured global DNA methylation (whole-genome bisulfite sequencing) in F₀, F₂, and F₃ generations. Detecting epigenetic changes and elevated insecticide tolerance in the F₃ generation is particularly significant, because it would signify inheritance without direct stress exposure. To test for the association between methylation and phenotype at each step, we additionally assessed transcriptomic diversity (RNA sequencing) and individual performance (larval mobility, larval feeding rate, larval development time, pupal weight, and adult weight). We accounted for genomic ancestry by tracing the parentage of all beetles across generations. Our findings will help identify the underlying eco-evolutionary mechanisms facilitating establishment and spread of CPB and other agricultural insect pests. Such knowledge may contribute to developing innovative approaches for mitigation and pest removal and for ensuring agroecological sustainability.