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

Crop
pollination by the western honey bee Apis
mellifera 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 Varroa destructor, 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.