Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants

Division of labor (DOL) is a characteristic trait of insect societies, where tasks are generally performed by specialized individuals. Inside workers focus on brood or nest care, while others take risks by foraging outside. Theory proposes that workers have different thresholds to perform certain tasks when confronted with task-related stimuli, leading to specialization and consequently DOL. Workers are presumed to vary in their response to task-related cues rather than in how they perceive such information. Here, we test the hypothesis that DOL instead stems from workers varying in their efficiency to detect stimuli of specific tasks. We use transcriptomics to measure mRNA expression levels in the antennae and brain of nurses and foragers of the ant Temnothorax longispinosus. We find seven times as many genes to be differentially expressed between behavioral phenotypes in the antennae compared to the brain. Moreover, nearly half of all odorant receptors are differentially expressed, with an overrepresentation of the 9-exon gene family upregulated in the antennae of nurses. Nurses and foragers thus apparently differ in the perception of their olfactory environment and task-related signals. Our study supports the hypothesis that antennal sensory filters predispose workers to specialize in specific tasks.

劳动分工（Division of Labor，DOL）是昆虫社会的典型特征，各类任务通常由特化的个体承担。内勤工蚁主要负责育幼与巢群维护，外勤工蚁则承担外出觅食的高风险工作。现有理论提出，工蚁在接触任务相关刺激时，完成特定任务的阈值存在差异，这会推动个体特化，最终形成劳动分工。此前的研究推测，工蚁之间的差异源于对任务相关线索的响应强度不同，而非对这类信息的感知方式存在区别。本研究旨在验证一项与该理论不同的假说：劳动分工实则源于工蚁在检测特定任务相关刺激的效率上存在差异。我们以长刺盘胸蚁（Temnothorax longispinosus）为研究对象，利用转录组学（transcriptomics）技术检测了其内勤工蚁与外勤工蚁触角和大脑中的信使RNA（mRNA）表达水平。研究结果显示，相较于大脑，触角在两种行为表型间的差异表达基因数量是大脑的7倍。此外，近半数的嗅觉受体基因存在差异表达，其中内勤工蚁触角中的9外显子基因家族呈现显著富集且上调表达。由此可见，内勤工蚁与外勤工蚁在嗅觉环境感知以及任务相关信号的识别上存在显著差异。本研究证实了这一假说：触角的感官过滤机制会促使工蚁特化并承担特定任务。