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.

西方蜜蜂（Apis mellifera）介导的作物授粉对农业生产至关重要，但却正面临着蜂群死亡率居高不下的严峻威胁，这一问题在欧洲与美国尤为突出。蜂群损失的部分诱因，是由体外寄生螨瓦螨（Varroa destructor）传播的变形翼病毒（Deformed wing virus, DWV）高载量感染，尤其在蜂群越冬阶段危害更为显著。隐性DWV感染极为普遍，且已被证实与蜜蜂过早出巢觅食存在因果关系，而该行为又与蜂群损失密切相关。研究团队依托四项意外发现隐性DWV-A感染证据的大脑转录组研究，旨在探究该效应是否源于DWV-A模拟了与蜜蜂行为成熟相关的大脑基因表达自然变化。研究结果与该假说相符：即便样本蜜蜂的日龄远低于典型觅食蜂，DWV-A感染蜜蜂的大脑基因表达谱仍与觅食蜂高度相似。此外，转录调控网络分析显示，DWV-A感染与此前被证实与蜜蜂觅食行为相关的转录因子呈正相关关系。令人意外的是，单细胞RNA测序（single-cell RNA-Sequencing）表明，该效应的核心介导者为神经胶质细胞而非神经元——昆虫大脑中的神经胶质细胞本就数量稀少，且极少与行为可塑性相关联。隐性DWV-A感染还与蜜蜂学习能力受损存在关联，结合过早出巢觅食的行为，这可能会导致在现代密集养蜂场环境下，不同蜂群间蜜蜂误群加入的概率显著上升。综上，上述研究结果支持了DWV-A可通过调控宿主行为以促进病毒水平传播的机制性关联。