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, Apis cerana(Ac), formed heat balls in response to Ac and hornet (Vespavelutina) alarm pheromones, demonstrating eavesdropping. The allopatric species, Apismellifera(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, (E)-2-decen-1-yl acetate, and benzyl acetate. Only Ac heat-balled in response to realistic bee alarm pheromone component levels, <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.据推测，窃听行为会在同域分布而非异域分布的捕食者与猎物之间演化形成。亚洲蜜蜂与其天敌胡蜂之间的演化军备竞赛，催生了一种极为精妙的防御策略——热球防御（heat-balling），该策略通过热量与二氧化碳使胡蜂窒息。我们的研究表明，同域分布的亚洲物种东方蜜蜂（Apis cerana，简称Ac）会在感知到自身与胡蜂（Vespavelutina）的报警信息素后形成热球，从而证实了其具备窃听行为。而异域分布的西方蜜蜂（Apis mellifera，简称Am）仅对活体胡蜂与自身的报警信息素产生微弱反应，却无法感知胡蜂的报警信息素。当守卫蜂最初发起攻击时，我们观察到了典型的胡蜂报警信息素释放行为——胡蜂蜇针伸出。热球形成后，守卫蜂会释放蜜蜂蜇针报警信息素，包括乙酸异戊酯、乙酸辛酯、(E)-2-癸烯-1-基乙酸酯以及乙酸苄酯。仅当乙酸异戊酯的浓度达到符合自然场景的蜜蜂报警信息素水平（低于1只蜜蜂等效剂量，即1 μg）时，东方蜜蜂才会形成热球。细致的窃听实验表明，东方蜜蜂会对胡蜂报警信息素的人工合成混合物作出热球反应，而西方蜜蜂则不会。仅东方蜜蜂的触角对胡蜂报警信息素成分与毒液挥发物表现出强烈且稳定的反应。本研究数据首次证实，同域分布的东方蜜蜂能够窃听胡蜂的报警信息素，并结合自身的报警信息素信号，以此发起热球防御；而异域分布的西方蜜蜂则不具备这一能力。演化过程大概率赋予了东方蜜蜂这种窃听能力，这是异域分布的西方蜜蜂所不具备的适应性特征。