Data from: Plant defenses against ants provide a pathway to social parasitism in butterflies

Understanding the chemical cues and gene expressions that mediate herbivore-hostplant and parasite-host interactions can elucidate the ecological costs and benefits accruing to different partners in tight-knit community modules, and may reveal unexpected complexities. We investigated the exploitation of sequential hosts by the phytophagous-predaceous butterfly Maculinea arion, whose larvae initially feed on Origanum vulgare flowerheads before switching to parasitize Myrmica ant colonies for their main period of growth. Gravid female butterflies were attracted to Origanum plants that emitted high levels of the monoterpenoid volatile carvacrol, a condition that occurred when ants disturbed their roots: we also found that Origanum expressed four genes involved in monoterpene formation when ants were present, accompanied by a significant induction of jasmonates. When exposed to carvacrol, Myrmica workers upregulated five genes whose products bind and detoxify this biocide, and their colonies were more tolerant of it than other common ant genera, consistent with an observed ability to occupy the competitor-free spaces surrounding Origanum. A cost is potential colony destruction by Maculinea arion, which in turn may benefit infested Origanum plants by relieving their roots of further damage. Our results suggest a new pathway whereby social parasites can detect successive resources by employing plant volatiles to simultaneously select their initial plant food and a suitable sequential host.

解析介导植食者-寄主植物以及寄生物-寄主互作的化学信号与基因表达，可阐明紧密联结的群落模块中不同共生伙伴所面临的生态成本与收益，亦能揭示此前未被认知的复杂互作关系。本研究针对兼具植食性与拟寄生性的大蓝蝶（Maculinea arion）开展研究，该蝶幼虫初始取食牛至（Origanum vulgare）的花序，随后转而寄生红蚁属（Myrmica）蚁群以完成其主要生长阶段。怀卵雌蝶会被释放高含量单萜类挥发性物质香芹酚（carvacrol）的牛至植株所吸引，而当蚁群扰动牛至根部时，植株便会释放该物质；研究同时发现，当蚁群存在时，牛至会激活4个参与单萜合成的基因，同时茉莉酸类（jasmonates）物质的表达量显著上调。当红蚁工蚁暴露于香芹酚环境时，会上调5个编码结合并降解该生物毒素的蛋白的基因；且红蚁蚁群对香芹酚的耐受性显著高于其他常见蚁属，这与其可占据牛至周边无竞争生态位的观测结果相符。该互作存在潜在代价：红蚁蚁群可能被大蓝蝶幼虫破坏，而这反过来可通过减轻牛至根部的进一步损伤，使受侵染的牛至植株获益。本研究结果揭示了一条全新的互作路径：社会性寄生物可通过利用植物挥发性物质，同时筛选其初始植食寄主与后续适宜的共生宿主。