Integrative assessment of sulfoxaflor effects on gene expression, reproduction, and behavior in the bumblebee Bombus impatiens

Social insect pollinators, such as bumblebees, face increasing threats from environmental agrochemicals; yet the sublethal effects of these compounds across different levels of biological organization remain poorly understood. This study uses an integrative approach to examine how chronic exposure to sublethal concentrations of the insecticide sulfoxaflor affects the common eastern bumblebee (Bombus impatiens). Microcolonies of B. impatiens worker bees were fed sulfoxaflor-treated sugar water for 21 days. We then assessed changes in molecular, physiological, and behavioral traits resulting from sulfoxaflor exposure. Transcriptomic analysis revealed extensive differential gene expression in ovaries, but not brains, of exposed bees. Bees exposed to sulfoxaflor showed upregulated cellular signaling pathways and downregulated genes associated with oogenesis and mitosis. Moreover, sulfoxaflor-exposed bees showed reduced tissue-biased gene expression, suggesting broader disruption in tissue-specific regulation. At the physiological level, exposed workers exhibited disrupted ovarian development and produced significantly fewer eggs. In addition, sulfoxaflor-exposed bees displayed significantly increased stinging behavior and decreased leg lifting behavior. Finally, exposed microcolonies exhibited reduced sugar water consumption and impaired nest building. Overall, these results indicate that reproductive tissues are more sensitive to sulfoxaflor exposure than neural tissues and that molecular disruptions manifest in impaired physiology and colony-level behaviors. This study highlights the value of assessing multiple levels of biological organization when investigating the nonlethal yet ecologically significant effects of agrochemicals on pollinator health.