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 synthesisdependent 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.egg parasitoid ͉ memory ͉ phoresy ͉ Pieris ͉ Trichogramma

Chemical Ecology of Egg Parasitoids Associated with True Bugs

“…First, parasitoids may detect volatiles from nontarget instars of the host, that is, adults or juveniles, to reach the vicinity of the host eggs (infochemical detour sensu Vet & Dicke [8]), eventually enabling them to pin-point eggs using additional long-and/or short-range cues. A particular and interesting example of such detour behavior of egg parasitoids is phoresy on adult host females; via this strategy, not only are relevant cues more detectable, but the adult itself is also exploited by the parasitoid as a vehicle to arrive at host eggs [15][16][17]. Second, parasitoids may exploit plant volatiles induced as a consequence of herbivory, which are emitted in large quantities and are, therefore, easily detectable by foraging parasitoids but not necessarily highly reliable [13].…”

Nocturnal parasitism of moth eggs byTrichogrammawasps

“…Trichogramma wasps also generally have more than 24 hours time to parasitise nocturnally laid host eggs until the head of the host's caterpillar has sclerotised. Diurnal activity has been shown for many Trichogramma species, and also for the strains used in this study (Woelke & Huigens, personal observations and, for example, Fatouros, Broekgaarden, et al, 2008;Fatouros, Bukovinszkine'Kiss et al, 2005;Fatouros et al, 2007;Fatouros, Huigens, et al, 2005;Huigens et al, 2009Huigens et al, , 2010Huigens et al, , 2011Woelke, 2008). Reznik et al (2009) found for T. principium Sug.…”

“…Only under limited host conditions (which is not the case in our study) superparasitism may occasionally occur: two wasp eggs allocated in one E. kuehniella egg may then result in two emerging wasps (M. E. Huigens, personal observations). Wasps of all strains are known to parasitise eggs in the photophase during daytime (Woelke & Huigens, personal observations;Fatouros, Broekgaarden, et al, 2008;Fatouros, Bukovinszkine'Kiss, et al, 2005, Fatouros, Huigens, et al, 2005Huigens et al, 2009Huigens et al, , 2010.…”

“…These strains have previously been discriminated by a molecular key based on the Internal Transcribed Spacer 2 gene region (Stouthamer, Hu, van Kan, Platner, & Pinto, 1999, sequences are available in an extensive electronic database with ITS-2 sequences of Trichogramma wasps managed by Prof. Richard Stouthamer at the University of California, Riverside, USA) and were used in previous diurnal studies (Fatouros, Bukovinszkine'-Kiss, Dicke, & Hilker, 2007;Fatouros, Broekgaarden, et al, 2008;Fatouros, Bukovinszkine'Kiss, et al, 2005, Fatouros, Huigens, et al, 2005Huigens, de Swart, & Mumm, 2011;Huigens et al, 2009Huigens et al, , 2010. Iso-female strain Y175 originated from a vegetable garden in Lienden, The Netherlands, and was collected from a paper card with eggs of the cabbage moth Mamestra brassicae L. (Lepidoptera: Noctuidae) attached to a cabbage plant in the summer of 1999.…”

“…those induced by host egg deposition) (for a review, see Fatouros, Dicke, Mumm, Meiners, & Hilker, 2008). Although the wasps may find lepidopteran host eggs mainly by walking and flying short distances within a host habitat, some species may also hitch-hike with adult butterflies and moths to disperse over longer distances and/or to obtain immediate access to freshly laid host eggs Fatouros, Huigens, van Loon, Dicke, & Hilker, 2005;Huigens & Fatouros, 2013;Huigens et al, 2009Huigens et al, , 2010. We expect that this phoretic behaviour may also occur at low temperatures at night.…”