Susceptibility to the Neonicotinoid Pesticide Imidacloprid Is Linked to Life History Regulation in Honey Bees ( Apis mellifera L.)

The Western honey bee (Apis mellifera) is a globally important pollinator. Its health in natural and managed populations is compromised by numerous factors, including pesticides. Neonicotinoid pesticides are widely used even though they can cause a variety of detrimental effects. Exposure can disrupt the complex life history regulation of worker honey bees and induce precocious foraging and premature death. However, honey bee variation in neonicotinoid susceptibility and underlying mechanisms are poorly understood. We hypothesised that neonicotinoid susceptibility and life history of worker honey bees are innately linked through constitutive patterns of gene expression. We confirmed the relation between worker survival of an acute exposure to the neonicotinoid imidacloprid and the inherent rate of the workers' most fundamental life history transition from in-hive tasks to initiate foraging in a colony-level experiment. To investigate the underlying mechanisms, we also compared the whole-body transcriptomes of young nurses, young foragers, old nurses, and old foragers between bees from colony sources with low versus high imidacloprid susceptibility that were raised in a common single cohort colony environment. These comparisons identified age- and behaviour-related transcriptome changes that are consistent with current models of the life history regulation of honey bee workers but also indicated that age itself has a profound effect on the whole-body transcriptome. Importantly, hundreds of gene expression changes distinguished honey bees of low and high imidacloprid susceptibility, largely in an age- and caste-specific manner with the most significant biological functions ranging from stress responses and protein homeostasis to apoptosis. General age and behavioural effects on the overall transcriptome correlated with each other, but the transcriptome differences according to imidacloprid susceptibility correlated with the age- and behaviour-related gene expression changes in an age-specific manner. However, significant directional overlap in differentially expressed genes from low and high imidacloprid susceptible bees existed among age and behavioural groups. Notably, three genes of known function differed consistently between bees of low and high imidacloprid susceptibility: A chitinase potentially providing structural resilience to pesticides, a potentially detoxifying cytochrome P450, and the vitellogenin receptor with putative functions in life history regulation and stress resistance in worker honey bees. These genes provide prime candidates for studying imidacloprid resistance in honey bees and other insects, as well as providing potential mechanistic links between pesticide effects and life history regulation.