Plant defences against ants provide a pathway to social parasitism in butterflies

TY - JOUR

T1 - Plant defences against ants provide a pathway to social parasitism in butterflies

AU - Patricelli, Dario

AU - Barbero, Francesca

AU - Occhipinti, Andrea

AU - Bertea, Cinzia M

AU - Bonelli, Simona

AU - Casacci, Luca P

AU - Zebelo, Simon A

AU - Crocoll, Christoph

AU - Gershenzon, Jonathan

AU - Maffei, Massimo E

AU - Thomas, Jeremy A

AU - Balletto, Emilio

PY - 2015/7/8

Y1 - 2015/7/8

N2 - 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.

AB - 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.

U2 - 10.1098/rspb.2015.1111

DO - 10.1098/rspb.2015.1111

M3 - Journal article

C2 - 26156773

SN - 0962-8452

VL - 282

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

IS - 1811

M1 - 20151111

ER -