Data from: Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leafcutter ants

Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.种植真菌的蚁群（fungus-farming ant colony）种群规模跨度可达4至5个数量级。它们会利用放线菌（actinomycete bacteria）与外分泌腺（exocrine glands）产生的化合物作为抗菌剂（antimicrobial agents）。切叶蚁属（Atta）蚁群拥有数百万只个体，对于研究蚁群卫生策略具有特殊意义——它们已摒弃了祖先对基于抗生素的生物防治的主要依赖，转而使用后胸侧板腺（metapleural gland, MG）的化学分泌物。切叶蚁属的后胸侧板腺能够合成大量苯乙酸（phenylacetic acid, PAA）——一种已被发现但研究甚少的抗菌剂，这一特性颇为独特。研究发现，在将苯乙酸主动涂抹至实验用菌圃片段的感染靶标，并将孢子转移至工蚁的口下囊（infrabuccal cavities）后，体型最小的工蚁可显著降低虫霉属（Escovopsis）与绿僵菌属（Metarhizium）孢子的萌发率。体外实验（in vitro assays）进一步表明，从演化衍生程度更高的切叶蚁中分离出的虫霉菌株，对苯乙酸的敏感性低于从系统发育更原始的种植真菌蚁类中分离的菌株，这一结果与虫霉属与宿主间的进化军备竞赛（evolutionary arms race）动态相符，但绿僵菌属则无此现象。相较于其他切叶蚁亚科（Attinae）类群，切叶蚁属蚁群规模更大，品级分化（caste differentiation）更为极端，且其社会几乎完全不存在生殖冲突。我们推测，这些特征与化学害虫防控领域独特的演化创新相关，而这类创新似乎能够抵御专性致病真菌（specialized mycopathogens）产生抗性的选择压力。