Evolved Eavesdropping: Sympatric But Not Allopatric Honey Bee Species Can Detect And Use Hornet Alarm Pheromone For Defence

Eavesdropping is predicted to evolve between sympatric, but not allopatric, predator and prey. The evolutionary arms race between Asian honey bees and their hornet predators has led to a remarkable defence, heat-balling, which suffocates hornets with heat and carbon dioxide. We show that the sympatric Asian species, <em>Apis cerana</em>(Ac), formed heat balls in response to Ac and hornet (<em>Vespa</em><em>velutina</em>) alarm pheromones, demonstrating eavesdropping. The allopatric species, <em>Apis</em><em>mellifera</em>(Am), only weakly responded to a live hornet and Am alarm pheromone, butnot to hornet alarm pheromone. We observed typical hornet alarm pheromone releasing behaviour, hornet sting extension, when guard bees initially attacked. Once heat balls were formed, guards released honey bee sting alarm pheromones: isopentyl acetate, octyl acetate, (<em>E</em>)-2-decen-1-yl acetate, and benzyl acetate. Only Ac heat-balled in response to realistic bee alarm pheromone component levels, &lt;1 bee-equivalent (1 µg), of isopentyl acetate. Detailed eavesdropping experiments showed that Ac, but not Am, formed heat-balls in response to a synthetic blend of hornet alarm pheromone. Only Ac antennae showed strong, consistent responses to hornet alarm pheromone compounds and venom volatiles. These data provide the first evidence that the sympatric Ac, but not the allopatric Am, can eavesdrop upon hornet alarm pheromone and uses this information, in addition to bee alarm pheromone, to heat-ball hornets. Evolution has likely given Ac this eavesdropping ability, an adaptation that the allopatric Am does not possess.窃听行为被预测会发生在同域分布（sympatric）而非异域分布（allopatric）的捕食者与猎物之间。亚洲蜜蜂与其胡蜂捕食者之间的进化军备竞赛，催生了一种极为精妙的防御策略——结球御敌（heat-balling），该策略通过热量与二氧化碳使胡蜂窒息。本研究证实，同域分布的亚洲物种<em>中华蜜蜂（Apis cerana，简称Ac）</em>会针对自身以及黄脚胡蜂（Vespa velutina）的告警信息素（alarm pheromones）发起结球御敌行为，证明其具备窃听能力。而异域分布的西方蜜蜂（Apis mellifera，简称Am）仅对活体胡蜂以及自身的告警信息素产生微弱响应，却无法识别胡蜂的告警信息素。当守卫蜂首次发起攻击时，我们观察到了胡蜂释放告警信息素的典型行为——螫针伸出（sting extension）。结球御敌行为形成后，守卫蜂会释放蜜蜂螫针告警信息素：乙酸异戊酯（isopentyl acetate）、乙酸辛酯（octyl acetate）、(E)-2-癸烯-1-基乙酸酯（(E)-2-decen-1-yl acetate）以及乙酸苄酯（benzyl acetate）。仅中华蜜蜂会针对符合自然浓度的蜜蜂告警信息素组分——乙酸异戊酯含量低于1蜂当量（1 μg）——发起结球御敌行为。后续细致的窃听实验表明，仅中华蜜蜂会针对人工合成的胡蜂告警信息素混合物发起结球御敌行为，西方蜜蜂则无此反应。仅中华蜜蜂的触角会对胡蜂告警信息素组分以及毒液挥发物产生强烈且稳定的响应。本研究数据首次提供证据表明，同域分布的中华蜜蜂能够窃听胡蜂的告警信息素，并结合蜜蜂自身的告警信息素，以此发起结球御敌行为对抗胡蜂；而异域分布的西方蜜蜂则不具备该能力。这一窃听能力大概率是进化赋予中华蜜蜂的适应性特征，而异域分布的西方蜜蜂并未演化出该特性。