Searching beyond the streetlight: Neonicotinoid exposure alters the neurogenomic state of worker honey bees

Neonicotinoid insecticides have been implicated in honey bee declines, with many studies showing that sublethal exposure impacts bee behaviors such as foraging, learning, and memory. Despite the large number of ecotoxicological studies carried out to date, most focus on a handful of worker phenotypes leading to a “streetlight effect” where the a priori choice of phenotypes to measure may influence the results and conclusions arising from the studies. This bias can be overcome with the use of toxicological transcriptomics, where changes in gene expression can provide a more objective view of how pesticides alter animal traits. Here, we used RNA sequencing to examine the changes in neurogenomic states of nurse and forager honey bees that were naturally exposed to neonicotinoids in the field and artificially exposed to neonicotinoids in a controlled experiment. We found that neonicotinoid exposure influenced the neurogenomic state of foragers and nurses in different ways; foragers experienced shifts in expression of genes involved in cognition and development, while nurses experienced shifts in expression of genes involved in metabolism. Our study suggests that neonicotinoids influence nurse and forager bees in a different manner. We also found no to minimal overlap in the differentially expressed genes in our study and in previously published studies, which might help reconcile the seemingly contradictory results often reported in the neonicotinoid literature.