Synergistic olfactory processing for social plasticity in desert locusts

Desert locust plagues threaten the food security of millions. Central to their formation is crowding-induced plasticity, with social phenotypes changing from cryptic (solitarious) to swarming (gregarious). Here, we elucidate the implications of this transition on foraging decisions and corresponding neural circuits. We use behavioral experiments and Bayesian modeling to decompose the multi-modal facets of foraging, revealing olfactory social cues as critical. To this end, we investigate how corresponding odors are encoded in the locust olfactory system using in-vivo calcium imaging. We discover crowding-dependent synergistic interactions between food-related and social odors distributed across stable combinatorial response maps. The observed synergy was specific to the gregarious phase and manifested in distinct odor response motifs. Our results suggest a crowding-induced modulation of the locust olfactory system that enhances food detection in swarms. Overall, we demonstrate how linking sensory adaptations to behaviorally relevant tasks can improve our understanding of social modulation in non-model organisms.沙漠蝗灾（Desert locust plagues）威胁着数百万人的粮食安全。蝗灾形成的核心机制是拥挤诱导的表型可塑性（crowding-induced plasticity）：社会性表型会从隐蔽型（独居型，solitarious）转变为群聚型（群居型，gregarious）。本研究阐明了这一表型转变对蝗虫觅食决策及其对应神经环路的影响。我们通过行为实验与贝叶斯建模（Bayesian modeling）拆解了觅食行为的多模态维度，发现嗅觉社交线索（olfactory social cues）是其中的关键调控因素。为此，我们借助活体钙成像（in-vivo calcium imaging）技术，探究了蝗虫嗅觉系统对相关气味的编码机制。研究发现，食物相关气味与社交气味之间存在依赖于种群密度的协同相互作用，该相互作用分布于稳定的组合响应图谱（combinatorial response maps）中。所观测到的协同效应仅特异性存在于群居型阶段，并表现出独特的气味响应基序（odor response motifs）。本研究结果表明，拥挤诱导的调控作用会重塑蝗虫的嗅觉系统，进而增强群居种群的食物探测能力。总体而言，本研究证实了将感官适应与行为相关任务相结合，能够深化我们对非模式生物（non-model organisms）社交调控机制的理解。