Understanding the chemical cues and gene expressions that mediate herbivore–host-plant 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
Ma. 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.
Bacterial communities within
Phengaris (Maculinea) alcon
caterpillars are shifted following transition from solitary living to social parasitism of
Myrmica
ant colonies
