School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK.
Department of Biology, University of Florence, Via Madonna del Piano 6, 50019 Sesto Fiorentino, Italy.
J Exp Biol. 2024 Jul 1;227(13). doi: 10.1242/jeb.246766. Epub 2024 Jul 10.
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.
病毒感染可能会损害西方蜜蜂（Apis mellifera）的觅食能力。变形翅膀病毒（DWV）是最常见的蜜蜂病毒，它被认为是导致学习和记忆障碍的一个可能原因。然而，到目前为止，这一现象的证据来自于人工感染的蜜蜂，而对于病毒的自然感染的影响知之甚少。我们利用触角延伸反射（PER），在一个简单的联想学习任务中，没有发现与自然 DWV 负荷之间有显著的关联。然而，通过反转联想学习测试，我们发现 DWV 负荷较高的蜜蜂在反转学习阶段表现更好。DWV 能够在蜜蜂的蘑菇体中复制，其中 GABA 能信号通路对联想学习有拮抗作用，但对反转学习至关重要。因此，我们评估了不同学习反应的蜜蜂中几种 GABA 相关基因的表达模式。有趣的是，蘑菇体中某些基因的表达与 DWV 负荷呈正相关，但仅与反转学习表现良好的蜜蜂有关。我们假设 DWV 可能通过增强对未奖励刺激的 GABA 抑制作用来提高嗅觉学习表现，这与我们观察到的行为模式一致。然而，在更高的疾病负担下，这种与 DWV 相关的 GABA 信号增加可能会损害联想学习，这与之前的其他研究一致。
