Yu Qiaoqiao, Yang Jing, Yu Jia, Lei Hong, Kang Le, Guo Xiaojiao
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
School of Life Sciences, Arizona State University, Tempe, AZ 85287.
Proc Natl Acad Sci U S A. 2025 Aug 19;122(33):e2501490122. doi: 10.1073/pnas.2501490122. Epub 2025 Aug 13.
Migratory locusts () emit two key odorants during aggregation: 4-vinylanisole (4VA), which serves as an aggregation pheromone attracting conspecifics to form swarms, and phenylacetonitrile (PAN), which acts as an aposematic signal and a precursor of a defense toxin, deterring conspecifics from cannibalism and protecting against predators. However, how locusts reconcile these two conflicting olfactory signals while aggregating is not yet understood. Our study addresses this by examining the release dynamics of the two signals, their behavioral effects, and the neural mechanisms underlying their perception. 4VA is released earlier and at lower locust densities than PAN, with PAN's release increasing as aggregation progresses. Although PAN's emission levels eventually exceed those of 4VA, locusts consistently exhibit a preference for the emitted blend, regardless of variations in proportions and concentrations. Notably, increasing amounts of 4VA added to PAN can counteract PAN's repellent effects, but this is not the case when PAN is added to 4VA. Mechanistically, we found that antennal neurons responsive to 4VA suppress the activity of neurons responsive to PAN. In the antennal lobe, it is the conduction velocities of projection neurons, rather than other neural properties, that are responsible for the observed behavioral pattern, leading to an overall attractive response. Collectively, our findings imply that insects are capable of harmonizing the effects of two distinct pheromones to optimize both social cohesion and chemical defense.
4-乙烯基苯甲醚（4VA），它作为一种聚集信息素，吸引同种个体形成群体；以及苯乙腈（PAN），它作为一种警戒信号和防御毒素的前体，阻止同种个体自相残杀并抵御捕食者。然而，蝗虫在聚集时如何协调这两种相互冲突的嗅觉信号尚不清楚。我们的研究通过研究这两种信号的释放动态、它们的行为效应以及其感知背后的神经机制来解决这个问题。4VA比PAN释放得更早，且在蝗虫密度较低时就开始释放，随着聚集过程的推进，PAN的释放量增加。尽管PAN的释放水平最终超过了4VA，但蝗虫始终对释放出的混合气味表现出偏好，无论比例和浓度如何变化。值得注意的是，向PAN中添加越来越多的4VA可以抵消PAN的驱避作用，但将PAN添加到4VA中时情况并非如此。从机制上讲，我们发现对4VA有反应的触角神经元会抑制对PAN有反应的神经元的活动。在触角叶中，是投射神经元的传导速度，而非其他神经特性，导致了观察到的行为模式，从而产生总体的吸引反应。总的来说，我们的研究结果表明昆虫能够协调两种不同信息素的作用，以优化社会凝聚力和化学防御。
