Conspecific mortality cues mediate associative learning in crickets, Acheta domesticus (Orthoptera: Gryllidae)

Abstract

Many terrestrial and aquatic animals learn associations between environmental features and chemical cues of mortality risk (e.g. conspecific alarm pheromones or predator-derived cues), but the chemical nature of the cues that mediate this type of learning are rarely considered. Fatty acid necromones (particularly oleic and linoleic acids) are well established as cues associated with dead or injured conspecifics. Necromones elicit risk aversive behavior across diverse arthropod phylogenies, yet they have not been linked to associative learning. Here, we provide evidence that necromones can mediate associative olfactory learning in an insect by acting as an aversive reinforcement. When house crickets (Achetadomesticus) were forced to inhabit an environment containing an initially attractive odor along with a necromone cue, they subsequently avoided the previously attractive odor and displayed tolerance for an initially unattractive odor. This occurred when crickets were conditioned with linoleic acid but not when they were conditioned with oleic acid. Similar aversive learning occurred when crickets were conditioned with ethanol body extracts composed of male and female corpses combined, as well as extracts composed of female corpses alone. Conditioning with male body extract did not elicit learned aversion in either sex, even though we detected no notable differences in fatty acid composition between male and female body extracts. We suggest that necromone-mediated learning responses might vary depending on synergistic or antagonistic interactions with sex or species-specific recognition cues.