Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense

Abstract

Plants can recruit parasitic wasps in response to egg deposition by herbivorous insects-a sophisticated indirect plant defense mechanism. Oviposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprout plants induces phytochemical changes that arrest the egg parasitoid Trichogramma brassicae. Here, we report the identification of an elicitor of such an oviposition-induced plant response. Eliciting activity was present in accessory gland secretions released by mated female butterflies during egg deposition. In contrast, gland secretions from virgin female butterflies were inactive. In the male ejaculate, P. brassicae females receive the anti-aphrodisiac benzyl cyanide (BC) that reduces the females' attractiveness for subsequent mating. We detected this pheromone in the accessory gland secretion released by mated female butterflies. When applied onto leaves, BC alone induced phytochemical changes that arrested females of the egg parasitoid. Microarray analyses revealed a similarity in induced plant responses that may explain the arrest of T. brassicae to egg-laden and BC-treated plants. Thus, a male-derived compound endangers the offspring of the butterfly by inducing plant defense. Recently, BC was shown to play a role in foraging behavior of T. brassicae, by acting as a cue to facilitate phoretic transport by mated female butterflies to oviposition sites. Our results suggest that the anti-aphrodisiac pheromone incurs fitness costs for the butterfly by both mediating phoretic behavior and inducing plant defense.