Sublethal Exposure Effects of the Neonicotinoid Clothianidin Strongly Modify the Brain Transcriptome and Proteome in the Male Moth Agrotis ipsilon

SIMPLE SUMMARY: Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids such as clothianidin. Low doses of insecticides can stimulate various life traits in target pest insects, whereas negative effects are expected. We recently showed that treatments with different low doses of clothianidin could modify behavioral and neuronal sex pheromone responses in the male moth, Agrotis ipsilon. In this study, we showed that clothianidin disrupted 1229 genes and 49 proteins at the molecular level, including numerous enzymes of detoxification and neuronal actors, which could explain the acclimatization in pest insects to the insecticide-contaminated environment. ABSTRACT: Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids such as clothianidin. The residual accumulation of low concentrations of these insecticides can have positive effects on target pest insects by enhancing various life traits. Because pest insects often rely on sex pheromones for reproduction and olfactory synaptic transmission is cholinergic, neonicotinoid residues could indeed modify chemical communication. We recently showed that treatments with low doses of clothianidin could induce hormetic effects on behavioral and neuronal sex pheromone responses in the male moth, Agrotis ipsilon. In this study, we used high-throughput RNAseq and proteomic analyses from brains of A. ipsilon males that were intoxicated with a low dose of clothianidin to investigate the molecular mechanisms leading to the observed hormetic effect. Our results showed that clothianidin induced significant changes in transcript levels and protein quantity in the brain of treated moths: 1229 genes and 49 proteins were differentially expressed upon clothianidin exposure. In particular, our analyses highlighted a regulation in numerous enzymes as a possible detoxification response to the insecticide and also numerous changes in neuronal processes, which could act as a form of acclimatization to the insecticide-contaminated environment, both leading to enhanced neuronal and behavioral responses to sex pheromone.