Host-mediated insecticide sequestration in target-site-resistant pests impacts parasitoid fitness and evolution

Insecticide resistance poses a major challenge to global pest management, yet its cascading effects on ecological networks remain poorly understood. Here, we show that target-site-resistant herbivorous insects can accumulate unmetabolized insecticides and inadvertently function as "toxic prey," impairing the fitness of their natural enemies. Using neonicotinoid- and spinosyn-resistant Myzus persicae and genetically modified Drosophila melanogaster, we demonstrate that resistant hosts surviving high-dose insecticide exposure retain substantial poison residues that are transferred to developing parasitoids. This host-mediated exposure leads to reduced parasitoid emergence, shortened adult lifespan, and smaller body size, even persisting across generations. Moreover, we identify parallel evolution of resistance-conferring Rdl (resistance to dieldrin) mutations in multiple distantly related parasitoid species that target cyclodiene- and fipronil-resistant hosts. This mirrors the coevolutionary arms race seen in natural systems, where the same genetic mutations that allow herbivores to tolerate plant toxins also enable their predators to overcome those defenses. By uncovering a consequential route of insecticide exposure via trophic transfer, and the resulting coadaptation in higher trophic levels, our study offers critical insights into the ecological costs of resistance and highlights the need for pest management strategies that integrate both chemical and biological control sustainably.