The Combined Effects of Varroa destructor Parasitism and Exposure to Neonicotinoids Affects Honey Bee (Apis mellifera L.) Memory and Gene Expression

Abstract

Honey bees (Apis mellifera L.) are exposed biotic and abiotic stressors but little is known about their combined effect and impact on neural processes such as learning and memory, which could affect behaviours that are important for individual and colony survival. This study measured memory with the proboscis extension response (PER) assay as well as the expression of neural genes in bees chronically exposed to three different sublethal doses of the insecticide clothianidin and/or the parasitic mite Varroa destructor. The proportion of bees that positively responded to PER at 24 and 48 h post-training (hpt) was significantly reduced when exposed to clothianidin. V. destructor parasitism reduced the proportion of bees that responded to PER at 48 hpt. Combined effects between the lowest clothianidin dose and V. destructor for the proportion of bees that responded to PER were found at 24 hpt. Clothianidin, V. destructor and their combination differentially affected the expression of the neural-related genes, AmNrx-1 (neurexin), AmNlg-1 (neuroligin), and AmAChE-2 (acetylcholinesterase). Different doses of clothianidin down-regulated or up-regulated the genes, whereas V. destructor tended to have a down-regulatory effect. It appears that clothianidin and V. destructor affected neural processes in honey bees through different mechanisms.