Juvenile hormone pathway in honey bee larvae: a source of possible signal molecules for the reproductive behavior of Varroa destructor

The parasitic mite Varroa destructor devastates honey bee (Apis mellifera) colonies around the world. Entering a brood cell shortly before capping, the Varroa mother feeds on the honey bee larvae. The hormones 20-hydroxyecdysone (20E) and juvenile hormone (JH), acquired from the host, have been considered to play a key role in initiating Varroa's reproductive cycle. This study focuses on differential expression of the genes involved in the biosynthesis of JH and ecdysone at 6 time points during the first 30 hours after cell capping in both drone and worker larvae of A. mellifera. This time frame, covering the conclusion of the honey bee brood cell invasion and the start of Varroa's ovogenesis, is critical to the successful initiation of a reproductive cycle. Our findings support a later activation of the ecdysteroid cascade in honey bee drones compared to worker larvae, which could account for the increased egg production of Varroa in A. mellifera drones. The JH pathway was generally downregulated confirming its activity is antagonistic to the ecdysteroid pathway during the larva development. Nevertheless, the genes involved in JH synthesis revealed an increased expression in drones. The upregulation of jhamt gene involved in methyl farnesoate (MF) synthesis came into attention since the MF is not only a precursor of JH but it is also an insect pheromone in its own right as well as JH-like hormone in Acari. This could indicate a possible kairomone effect of MF for attracting the mites into the drone brood cells, along with its potential involvement in ovogenesis after the cell capping, stimulating Varroa's initiation of egg laying.

寄生螨狄斯瓦螨（Varroa destructor）会对全球范围内的西方蜜蜂（Apis mellifera）蜂群造成毁灭性危害。该雌螨会在蜜蜂幼虫房封盖前不久侵入房内，取食蜜蜂幼虫。此前学界认为，从宿主体内获取的20-羟基蜕皮酮（20-hydroxyecdysone, 20E）与保幼激素（juvenile hormone, JH），在启动狄斯瓦螨生殖周期的过程中扮演关键角色。本研究聚焦于西方蜜蜂雄蜂与工蜂幼虫在幼虫房封盖后前30小时内的6个时间节点中，参与保幼激素与蜕皮激素生物合成的基因的差异表达情况。该时间窗口覆盖了狄斯瓦螨完成蜂房侵入至其卵子发生启动的完整阶段，对于生殖周期的成功启动至关重要。研究结果显示，与工蜂幼虫相比，西方蜜蜂雄蜂体内的蜕皮激素级联反应激活时间更晚，这或许可以解释狄斯瓦螨在西方蜜蜂雄蜂房内产卵量更高的现象。保幼激素通路整体呈现表达下调趋势，这印证了其在幼虫发育过程中与蜕皮激素通路相互拮抗的特性。不过，雄蜂体内参与保幼激素合成的基因表达量却有所升高。其中，参与法尼酸甲酯（methyl farnesoate, MF）合成的jhamt基因的上调表达值得关注：法尼酸甲酯不仅是保幼激素的前体物质，本身也是一种昆虫信息素，同时在蜱螨亚纲生物中兼具保幼激素类似物的活性。这一发现提示，法尼酸甲酯可能通过利它素效应吸引狄斯瓦螨侵入雄蜂幼虫房，同时在幼虫房封盖后参与卵子发生过程，进而刺激狄斯瓦螨启动产卵。