The evolutionary origin of queen pheromones (QPs), which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect QPs—such as cuticular hydrocarbons—were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on preexisting gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee QP pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.

中文翻译：

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大黄蜂中蜜蜂女王下颌信息素的交叉活性为感觉开发提供了证据

女王信息素（QPs）的进化起源调节昆虫社会中的生殖分工，已通过两个进化场景进行了解释：发送者前体假说和感官利用假说。这些情况在信号发送系统是基于发送方女王还是接收方工作者的预适应方面有所不同。虽然一些社会昆虫的QP（例如表皮碳氢化合物）很可能是从祖先的繁殖线索衍生而来的，并且根据前一种理论进化而成的，但蜜蜂的女王下颌信息素（QMP）已被建议直接作用于与繁殖相关的预先存在的基因调控网络。事实证明，QMP还可以抑制果蝇的卵巢活化，从而暗示利用保守的生理途径。为了验证QMP对更紧密相关的社会社会物种是否具有相似的影响，我们在这里测试了大黄蜂Bombus terrestris中的QMP交叉活性。有趣的是，我们发现非天然QMP混合物显着抑制了工蜂和大黄蜂的产卵，并引起了卵巢激活的伴随变化。相比之下，本地大黄蜂QP pentacosane只能抑制工人的繁殖。总的来说，这些发现支持了蜜蜂QMP可能通过感觉开发途径进化的假设。我们认为，这种剥削可以使社交昆虫皇后产生能够操纵工人保持无菌状态的化合物，但主要障碍在于，皇后本身必须对此类化合物具有免疫力。