Learning Performance and GABAergic Pathway Link to Deformed Wing Virus in the Mushroom Bodies of Naturally Infected Honey Bees

ABSTRACT Viral infections can be detrimental to the foraging ability of the western honey bee, Apis mellifera. The deformed wing virus (DWV) is the most common honey bee virus and has been proposed as a possible cause of learning and memory impairment. However, evidence for this phenomenon so far has come from artificially infected bees, while less is known about the implications of natural infections with the virus. Using the proboscis extension reflex (PER), we uncovered no significant association between a simple associative learning task and natural DWV load. However, when assessed through a reversal associative learning assay, bees with higher DWV load performed better in the reversal learning phase. DWV is able to replicate in the honey bee mushroom bodies, where the GABAergic signalling pathway has an antagonistic effect on associative learning but is crucial for reversal learning. Hence, we assessed the pattern of expression of several GABA-related genes in bees with different learning responses. Intriguingly, mushroom body expression of selected genes was positively correlated with DWV load, but only for bees with good reversal learning performance. We hypothesise that DWV might improve olfactory learning performance by enhancing the GABAergic inhibition of responses to unrewarded stimuli, which is consistent with the behavioural patterns that we observed. However, at higher disease burdens, which might be induced by an artificial infection or by a severe, natural Varroa infestation, this DWV-associated increase in GABA signalling could impair associative learning as previously reported by other studies.