Origanum vulgare terpenoids modulate Myrmica scabrinodis brain biogenic amines and ant behaviour

Coordinated social behaviour is fundamental for ant ecological success. However, even distantly-related organisms, such as plants, have evolved the ability to manipulate ant collective performances to their own advantage. In the parasitic system encompassing Maculinea butterflies, Myrmica ants, and Origanum vulgare plants, the ant-plant interaction elicits the release of a volatile terpenoid compound (carvacrol) which is used by the gravid butterfly to locate the ideal oviposition site. Here we show that this ant-plant association is maintained by the effect of O. vulgare terpenoids on ant behaviour and that food plants might gain protection by Myrmica ants by chemically manipulating workers to forage in their surroundings. The variation in the locomotor ability of three ant species (Formica cinerea, Tetramorium caespitum, and Myrmica scabrinodis) was studied after treatment with the two major O. vulgare terpenoid volatile compounds (i.e., carvacrol and thymol). The brain levels of three biogenic amines (dopamine, tyramine and serotonin) were analysed in ants exposed to the O. vulgare terpenoids by HPLC-ESI-MS/MS. Carvacrol and thymol increased the locomotor activity of all ant species tested, but if blended reduced the movement propensity of Myrmica scabrinodis. Dopamine and tyramine production was positively correlated with the worker locomotor activity. In Myrmica ants, both brain biogenic ammines were negatively correlated with the aggressive behaviour. Blends of O. vulgare volatiles affected the locomotor ability while increased the aggressiveness of Myrmica workers by altering the aminergic regulation in the ant brains. This behavioural manipulation, might enhance partner fidelity and plant protection. Our findings provide new insights supporting a direct role of plant volatiles in driving behavioural changes in social insects through biogenic amine modulation.协同社会行为是蚂蚁生态成功的关键基础。然而，即便亲缘关系较远的生物（如植物），也已演化出操控蚂蚁集体行为以谋取自身利益的能力。在由大蓝蝶（Maculinea）、红蚁属（Myrmica）蚂蚁以及牛至（Origanum vulgare）构成的寄生体系中，蚁植相互作用会诱导释放一种挥发性萜类化合物——香芹酚（carvacrol），该物质可被怀卵蝴蝶用于定位理想的产卵位点。 本研究证实，O. vulgare萜类化合物对蚂蚁行为的调控作用维持了这一蚁植共生关系，而食源植物或可通过化学手段操控工蚁在其周边觅食，从而获得红蚁属蚂蚁的保护。 研究针对三种蚂蚁——灰褐林蚁（Formica cinerea）、平胸切叶蚁（Tetramorium caespitum）以及粗节红蚁（Myrmica scabrinodis）——在经O. vulgare两种主要挥发性萜类化合物（即香芹酚（carvacrol）与百里香酚（thymol））处理后的运动能力变化展开了分析。通过高效液相色谱-电喷雾串联质谱（HPLC-ESI-MS/MS），检测了暴露于O. vulgare萜类化合物环境中的蚂蚁体内三种生物源性胺类（biogenic amines）：多巴胺（dopamine）、酪胺（tyramine）与血清素（serotonin）的脑内含量。 实验结果显示，香芹酚与百里香酚可提升所有受试蚂蚁物种的运动活性，但二者混合使用则会降低粗节红蚁的运动倾向。多巴胺与酪胺的生成量与工蚁运动活性呈正相关。在红蚁属蚂蚁中，两种脑内生物源性胺类均与攻击行为呈负相关。O. vulgare挥发性混合物可通过改变蚂蚁脑部的胺能调控机制，影响其运动能力，同时提升红蚁工蚁的攻击性。这种行为操控或可增强共生伙伴的忠诚度与植物保护效果。 本研究结果为植物挥发性物质通过调控生物源性胺类水平，推动社会性昆虫行为改变的直接作用提供了新的研究视角。