title: Plant defences against ants provide a pathway to social parasitism in butterflies.
abstract: 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.
authors.affiliation: Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, Turin 10123, Italy.
authors.forename: Dario
authors.initials: D
authors.lastname: Patricelli
authors.affiliation: Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, Turin 10123, Italy.
authors.forename: Francesca
authors.initials: F
authors.lastname: Barbero
authors.affiliation: Plant Physiology Unit, Department Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 15/A, Turin 10135, Italy.
authors.forename: Andrea
authors.initials: A
authors.lastname: Occhipinti
authors.affiliation: Plant Physiology Unit, Department Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 15/A, Turin 10135, Italy.
authors.forename: Cinzia M
authors.initials: CM
authors.lastname: Bertea
authors.affiliation: Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, Turin 10123, Italy.
authors.forename: Simona
authors.initials: S
authors.lastname: Bonelli
authors.affiliation: Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, Turin 10123, Italy.
authors.forename: Luca P
authors.initials: LP
authors.lastname: Casacci
authors.affiliation: Plant Physiology Unit, Department Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 15/A, Turin 10135, Italy.
authors.forename: Simon A
authors.initials: SA
authors.lastname: Zebelo
authors.affiliation: Department of Plant and Environmental Sciences, Faculty of Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark.
authors.forename: Christoph
authors.initials: C
authors.lastname: Crocoll
authors.affiliation: Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knoell-Strasse 8, Jena 07745, Germany.
authors.forename: Jonathan
authors.initials: J
authors.lastname: Gershenzon
authors.affiliation: Plant Physiology Unit, Department Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 15/A, Turin 10135, Italy.
authors.forename: Massimo E
authors.initials: ME
authors.lastname: Maffei
authors.affiliation: Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK jeremy.thomas@zoo.ox.ac.uk.
authors.forename: Jeremy A
authors.initials: JA
authors.lastname: Thomas
authors.affiliation: Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, Turin 10123, Italy.
authors.forename: Emilio
authors.initials: E
authors.lastname: Balletto
mesh_terms: D000818:Animals; D001000:Ants / Q000235:genetics / Q000469:parasitology* / Q000502:physiology*; D002080:Butterflies / Q000254:growth & development / Q000502:physiology*; D003463:Cues; D000081007:Cymenes; D005247:Feeding Behavior; D035264:Flowers / Q000378:metabolism; D005786:Gene Expression Regulation; D018506:Gene Expression Regulation, Plant; D006790:Host-Parasite Interactions; D007558:Italy; D007814:Larva / Q000254:growth & development / Q000502:physiology; D039821:Monoterpenes / Q000378:metabolism*; D031341:Origanum / Q000235:genetics* / Q000378:metabolism
chemical_list: D000081007:Cymenes; D039821:Monoterpenes; C073316:carvacrol
keywords: Maculinea; ant; gene expression; host detection; myrmecophily; plant volatiles