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. These include the deformed wing virus (DWV), which 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 loads. However, when assessed through a reversal associative learning assay, bees with higher DWV loads 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 hypothesize 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. Our results suggest that previously reported DWV-driven learning deficits might be exclusive to acute, artificial infections and do not occur in naturally infected bees, stressing the importance of investigating more ecologically relevant scenarios when assessing host-parasite systems. Summary statementThis study describes a virus-associated increase in learning in honey bees and proposes a mechanism based on GABA to explain the interplay between infection and cognition in the insect brain.