Molecular impact of Deformed wing virus type A in the honey bee brain.

Crop pollination by the western honey bee <i>Apis mellifera</i> is vital to agriculture but threatened by alarmingly high levels of colony mortality, especially in Europe and the US. Colony loss is due, in part, to the high viral loads of Deformed wing virus (DWV), transmitted by the ectoparasitic mite <i>Varroa destructor, </i>especially throughout the overwintering period of a honey bee colony. Covert DWV infection is commonplace and has been causally linked to precocious foraging, which itself has been linked to colony loss. Taking advantage of four brain transcriptome studies that unexpectedly revealed evidence of covert DWV-A infection, we set out to explore whether this effect is due to DWV-A mimicking naturally occurring changes in brain gene expression that are associated with behavioral maturation. Consistent with this hypothesis, we found that brain gene expression profiles of DWV-A infected bees resembled those of foragers, even in samples that were much younger than typical foragers. In addition, transcriptional regulatory network analysis revealed a positive association between DWV-A infection and transcription factors previously associated with honey bee foraging behavior. Surprisingly, single-cell RNA-Sequencing implicated glia, not neurons, in this effect; there are relatively few glial cells in the insect brain and they are rarely associated with behavioral plasticity. Covert DWV-A infection also has been linked to impaired learning, which together with precocious foraging can lead to increased occurrence of bees from one colony mistakenly joining another, especially under crowded modern apiary conditions. Together, these findings support a mechanistic link by which DWV-A may manipulate host behavior to facilitate horizontal transmission.