To locate their hosts, parasitic wasps can ‘eavesdrop’ on the intraspecific chemical communications of their insect hosts1,2,3. Here we describe an example in which the information exploited by the parasitic wasp Trichogramma brassicae is a butterfly anti-aphrodisiac that is passed from male to female Pieris brassicae butterflies during mating, to render them less attractive to conspecific males4,5,6. When the tiny wasp detects the odour of a mated female butterfly, it rides on her (Fig. 1) to her egg-laying sites and then parasitizes the freshly laid eggs. If this fascinating strategy is widespread in nature, it could severely constrain the evolution of sexual communication between hosts.
In two-choice olfactory bioassays (for methods, see supplementary information), females of the parasitic wasp T. brassicae showed a clear preference for odours of mated P. brassicae females or males (Fig. 2a). The wasps were more strongly attracted by the scents of male and mated female butterflies than of virgin females, but they did not discriminate between male and mated female butterflies. When offered separately against clean air, odours from male or mated female butterflies attracted the wasps significantly, but odours from virgin females did not (Fig. 2a).
In similar behavioural trials, we determined the concentration of the anti-aphrodisiac, benzyl cyanide5, that is attractive to the wasp. When given solvent-treated virgin females as an alternative, wasps were significantly attracted by odour from virgin female butterflies treated with 2 µg (P=0.008, Wilcoxon's matched pairs signed rank test) and 1 µg (P=0.016, Wilcoxon's matched pairs signed rank test) benzyl cyanide. This result indicates that T. brassicae is using the anti-aphrodisiac benzyl cyanide from P. brassicae as a foraging cue.
In further two-choice bioassays, we investigated whether wasps mount a mated female butterfly in response to the anti-aphrodisiac. When wasps were exposed to butterflies, they preferred to climb on to mated females rather than on to males or virgin females (Fig. 2b). Discrimination between males and mated females in this assay was probably based on close-range cues other than benzyl cyanide. But when virgin female butterflies painted with 2 µg benzyl cyanide dissolved in hexane were offered against virgin female butterflies painted with hexane alone, wasps preferred to mount the butterflies treated with benzyl cyanide significantly more often than the controls (Fig. 2b).
We used a flight chamber to determine whether T. brassicae wasps are transported by the mated female butterfly to the host plant, the Brussels sprout (Brassica oleracea var. gemmifera), where they subsequently parasitize her freshly laid eggs. In total, 28 mated female butterflies were each seen carrying a single wasp; 14 wasps (50%) were found on the butterfly after it had landed on the host plant and had started laying eggs. Four of these wasps reached the host plant by descending from the butterfly, and two of them parasitized the new eggs after leaving the butterfly. Transportation (phoresy) on female butterflies therefore led to successful parasitism by T. brassicae in at least 7.1% of cases.
Phoresy is an ambush strategy7,8 that has been only rarely observed in Trichogramma spp. (ref. 9; and N. E. F. and M. E. H., unpublished observations). But host location by chemical espionage in combination with phoresy, which we describe here, may have evolved frequently in egg parasitoids. From an egg parasitoid's point of view, it is most adaptive in those species with limited flight, a narrow time window for successful parasitism10, and/or a preference for hosts that lay egg clutches. From the host's perspective, egg parasitoids represent significant mortality factors11 and so exert selection on butterfly intraspecific communication, seriously constraining its evolution. The link between genetic variation in this important trait and local parasitoid selection pressure warrants further investigation.
Stowe, M. K., Turlings, T. C. J., Loughrin, J. H., Lewis, W. J. & Tumlinson, J. H. Proc. Natl Acad. Sci. USA 92, 23–28 (1995).
Arakaki, N., Wakamura, S. & Yasuda, T. J. Chem. Ecol. 22, 1079–1085 (1996).
Vinson, S. B. in Insect Communication (ed. Lewis, T.) 325–348 (Academic, London, 1984).
Andersson, J., Borg-Karlson, A. -K. & Wiklund, C. Proc. R. Soc. Lond. B 267, 1271–1275 (2000).
Andersson, J., Borg-Karlson, A. -K. & Wiklund, C. J. Chem. Ecol. 29, 1489–1499 (2003).
Gilbert, L. E. Science 193, 419–420 (1976).
Clausen, C. P. Annu. Rev. Entomol. 21, 343–368 (1976).
Bruni, R., Sant'Ana, J., Aldrich, J. R. & Bin, F. J. Insect Behav. 12, 165–173 (2000).
Tabata, S. & Tamanuki, K. Rev. Appl. Entomol. A 29, 95 (1940).
Orr, D. B., Russin, J. S. & Boethel, D. J. Can. Entomol. 118, 1063–1072 (1986).
Hilker, M. & Meiners, T. (eds) Chemoecology of Insect Eggs and Egg Deposition (Blackwell, Berlin, 2002).
The authors declare no competing financial interests.
About this article
Cite this article
Fatouros, N., Huigens, M., van Loon, J. et al. Butterfly anti-aphrodisiac lures parasitic wasps. Nature 433, 704 (2005). https://doi.org/10.1038/433704a
This article is cited by
Reverse chemical ecology in a moth: machine learning on odorant receptors identifies new behaviorally active agonists
Cellular and Molecular Life Sciences (2021)
Scientific Reports (2019)
Journal of Pest Science (2018)
Nature Communications (2017)
Maximized complexity in miniaturized brains: morphology and distribution of octopaminergic, dopaminergic and serotonergic neurons in the parasitic wasp, Trichogramma evanescens
Cell and Tissue Research (2017)