Indirect effects of insecticides on honey bee queens and their eggs via workers exposed to sublethal doses

Honey bees are the main agricultural crop pollinators and are constantly exposed to diverse agrochemicals including insecticides. Although queen, the sole reproductive individual in a colony, is protected from direct exposure to various stressors, she may indirectly be exposed to stressors through worker bees. Yet, little is known about the indirect effects of stressors on queens and their produced eggs. To address this knowledge gap, we assessed the effects of three widely used insecticides-acephate, bifenthrin, and chlorantraniliprole-on worker bees, with the aim to identify physiological changes in worker bees that could indirectly affect the physiology and reproductive traits of corresponding queens, as well as transcriptome alteration in their eggs. Our results revealed that exposure to acephate significantly reduced egg size, egg-laying activity, and queen weight, whereas no such changes were observed following exposure to chlorantraniliprole or bifenthrin. Additionally, acephate caused a significant inhibition of esterase activity in worker bees across all time intervals. Transcriptomic analysis revealed time-dependent changes in detoxification, immune- and antioxidant-related gene expression in workers, queens, and freshly laid eggs in response to all insecticides. These findings indicate that acephate can significantly alter the physiology of exposed worker bees, which would in turn indirectly affect the physiology and reproduction performance of corresponding queens, and ultimately extend to the next generation by altering the transcriptome profile of produced eggs.