Pheromone-induced accuracy of nestmate recognition in carpenter ants: simultaneous decrease of Type I and Type II errors

The ecological and evolutionary success of social insects relies on their ability to efficiently discriminate between group members and aliens. Nestmate recognition occurs by phenotype matching, the comparison of the referent (colony) phenotype to the one of an encountered individual. Based on the level of dissimilarity between the two, the discriminator accepts or rejects the target. The tolerated degree of mismatch is predicted by the acceptance threshold model, which assumes adaptive threshold shifts depending on the costs of discrimination errors. Inherent in the model is that rejection (Type I) and acceptance (Type II) errors are reciprocally related: if one type decreases, the other increases. We studied whether alarm pheromones modulate the acceptance threshold. We exposed Camponotus aethiops ants to formic acid and subsequently measured aggression towards nestmates and non-nestmates. Formic acid induced both more non-nestmate rejection and more nestmate acceptance than a control treatment, thus uncovering an unexpected effect of an alarm pheromone on responses to nestmates. Nestmate discrimination accuracy was improved via a decrease of both types of errors, a result that cannot be explained by a shift in the acceptance threshold. We propose that formic acid increases the amount of information available to the ants, thus decreasing the perceived phenotypic overlap between nestmate and non-nestmate recognition cues. This mechanism for improved discrimination reveals a novel function of alarm pheromones in recognition processes and may have far-reaching implications in our understanding of the modus operandi of recognition systems in general.

社会性昆虫（social insects）的生态与演化成功，有赖于其高效区分群体成员与外来个体的能力。巢友识别（nestmate recognition）依托表型匹配（phenotype matching）机制完成：即将参照群体的表型与偶遇个体的表型进行比对。依据二者的差异程度，识别者将选择接受或排斥目标个体。接受阈值模型（acceptance threshold model）可预测可容忍的错配程度，该模型假定适应性阈值偏移由识别错误的代价所决定。该模型的核心内涵在于，排斥错误（I型错误，Type I error）与接受错误（II型错误，Type II error）呈负相关关系：若一类错误降低，另一类则会升高。

我们针对告警信息素（alarm pheromone）是否可调控接受阈值展开了研究。我们将亮毛弓背蚁（Camponotus aethiops）暴露于甲酸（formic acid）环境中，随后测定其对巢友与非巢友的攻击行为。相较于对照组处理，甲酸处理组既表现出更强的非巢友排斥行为，也提升了对巢友的接受度，由此揭示了告警信息素对巢友识别反应的意外调控效应。本研究中，巢友识别准确率的提升源于两类识别错误的同时降低，这一结果无法通过接受阈值偏移得到合理解释。我们提出，甲酸可增加蚂蚁可获取的信息总量，进而缩小巢友与非巢友识别信号间的感知表型重叠度。这一优化识别的机制，揭示了告警信息素在识别过程中的全新功能，或可为我们全面理解各类生物识别系统的运作模式提供深远启示。