Hitch-hiking parasitic wasp learns to exploit butterfly antiaphrodisiac

Abstract

Many insects possess a sexual communication system that is vulnerable to chemical espionage by parasitic wasps. We recently discovered that a hitch-hiking (H) egg parasitoid exploits the antiaphrodisiac pheromone benzyl cyanide (BC) of the Large Cabbage White butterfly Pieris brassicae. This pheromone is passed from male butterflies to females during mating to render them less attractive to conspecific males. When the tiny parasitic wasp Trichogramma brassicae detects the antiaphrodisiac, it rides on a mated female butterfly to a host plant and then parasitizes her freshly laid eggs. The present study demonstrates that a closely related generalist wasp, Trichogramma evanescens, exploits BC in a similar way, but only after learning. Interestingly, the wasp learns to associate an H response to the odors of a mated female P. brassicae butterfly with reinforcement by parasitizing freshly laid butterfly eggs. Behavioral assays, before which we specifically inhibited long-term memory (LTM) formation with a translation inhibitor, reveal that the wasp has formed protein synthesis-dependent LTM at 24 h after learning. To our knowledge, the combination of associatively learning to exploit the sexual communication system of a host and the formation of protein synthesis-dependent LTM after a single learning event has not been documented before. We expect it to be widespread in nature, because it is highly adaptive in many species of egg parasitoids. Our finding of the exploitation of an antiaphrodisiac by multiple species of parasitic wasps suggests its use by Pieris butterflies to be under strong selective pressure.

Fig. 1.

Response of differently experienced T. evanescens wasps to odors of adults of the Large Cabbage White butterfly P. brassicae. Mean residence time (± SEM.) in the 2 odor fields of a 2-chamber olfactometer; n = 40 wasps tested per experiment; H, wasps were given an H experience 1 h before experiment; O, wasps were given an O experience 1 h before experiment; H+O, wasps were given an H experience followed by an O experience 1 h before experiment. Asterisks indicate significant differences within a choice test (Wilcoxon matched pairs signed-ranks test); **, P < 0.01; ***, P < 0.001; ns, not significant; a and b indicate significant differences between choice tests; 1, data of naive wasps are in agreement with previous work where another Dutch T. evanescens strain was used (27).

Fig. 2.

Mounting behavior of T. evanescens. (A) Proportion of first mounts of naive and experienced T. evanescens wasps on adults of the Large Cabbage White butterfly P. brassicae, the Small Cabbage White butterfly P. rapae, and young instars of the desert locust S. gregaria. Experienced wasps were given an H experience followed by an O experience (H+O) 1 h before the experiment; n = 40 climbing wasps tested per combination. (B) Female Trichogramma wasp of ≈0.5 mm touching the eye of a mated P. brassicae female (credits: Nina E. Fatouros, www.bugsinthepicture.com). Asterisks indicate significant differences within a choice test (binomial test); *, P < 0.05; ***, P < 0.001; ns, not significant; 1, data of naive wasps are in agreement with previous work where another Dutch T. evanescens strain was used (27).

Fig. 3.

Effects of the translation-inhibitor ANI on the response of T. evanescens wasps to odors of adults of the Large Cabbage White butterfly P. brassicae at 1 h and 24 h after a rewarding H experience (H+O). Mean residence time (± SEM.) in 2 odor fields in a 2-chamber olfactometer; n = 40 wasps tested per experiment; ANI, wasps were fed sucrose plus ANI before experience; C, control wasps were fed only sucrose before experience. Asterisks indicate significant differences within a choice test (Wilcoxon matched pairs signed-ranks test); ***, P < 0.001; ns, not significant.