Expression of foraging genes is associated with the division of labor among Western and Eastern honey bee adult workers

In the division of labor (DOL), individual bees exhibit varying behavioral responses to the same stimulus. Specifically, the response of adult worker bees to sucrose is highly variable and closely linked to differences in the behavioral decision-making. However, it is unclear whether patterns of gene-behavior interactions influence the DOL. In this study, we investigated the DOL mechanism in honeybee adult workers is associated with the sucrose responsiveness of bee foragers. First, we quantified the gustatory response scores (GRS) of the Western bee Apis mellifera and the Eastern bee Apis cerana under four tasks, that is, pollen foraging, nectar foraging, water foraging, and guarding. Second, we determined the mRNA levels of six forage-related genes in bees’ brains, namely the foraging genes Amfor and Acfor, which encode a cyclic guanosine monophosphate-dependent protein kinase, the dopamine receptor genes AmOct and AcOct, and the insulin receptor genes AmInR and AcInR. The results revealed that among Western bees, water and pollen foragers had the highest GRS. Among Eastern bees, water foragers had significantly higher GRS than nectar foragers. However, we observed no significant difference in the GRS between A. mellifera and A. cerana bee species under different tasks. The highest expression of foraging genes was detected in water foragers among A. mellifera species and guard bees among A. cerana species. Furthermore, we observed a significant positive correlation between foraging gene expressions and GRS in both Western and Eastern foragers. The results suggest that both bee species exhibit the same sensitivity in foraging for food in their ecological niches, and PKG signaling in the bees’ brain is directly linked to the DOL.

在分工协作（DOL）领域，个体蜜蜂对同一刺激表现出各异的行为反应。具体而言，成年工蜂对蔗糖的反应高度多变，且与行为决策的差异密切相关。然而，基因-行为相互作用模式是否影响分工协作尚不明确。在本研究中，我们探讨了蜜蜂成年工蜂的分工协作机制与其觅食者对蔗糖的敏感性之间的关联。首先，我们量化了西方蜜蜂 Apis mellifera 和东方蜜蜂 Apis cerana 在四项任务中的味觉反应评分（GRS），即花粉觅食、花蜜觅食、水觅食和守卫。其次，我们测定了蜜蜂大脑中与觅食相关的六种基因的mRNA水平，包括觅食基因Amfor和Acfor，它们编码一种环状鸟苷单磷酸依赖性蛋白激酶，多巴胺受体基因AmOct和AcOct，以及胰岛素受体基因AmInR和AcInR。研究结果显示，在西方蜜蜂中，水和花粉觅食者具有最高的GRS。在东方蜜蜂中，水觅食者的GRS显著高于花蜜觅食者。然而，我们在不同任务下观察到的A. mellifera 和 A. cerana 蜜蜂种群的GRS之间没有显著差异。在A. mellifera 种群中，水觅食者的觅食基因表达最高，而在A. cerana 种群中，守卫蜜蜂的觅食基因表达最高。此外，我们在西方和东方觅食者中观察到觅食基因表达与GRS之间存在显著的正相关关系。这些结果表明，两种蜜蜂物种在其生态位中觅食食物的敏感性相同，蜜蜂大脑中的PKG信号通路与分工协作直接相关。