An integrative and comparative study of aversive learning in two insect models, the fruit fly and the honeybee – INSAVEL

Aversive learning is an essential capacity that allows individual survival in a variable environment. It allows predicting that a given event is associated with a potential noxious stimulus so that appropriate, adaptive responding to this event is implemented. Aversive learning allows, therefore, survival in different natural conditions that range from predator avoidance to the rejection of unpalatable food sources. Insects have played a pivotal role for the study of learning and memory both at behavioral, cellular and molecular levels. In the case of aversive learning, the contributions made by insects have been so far limited to a single species, the fruit fly Drosophila melanogaster, and to a dominant, unique conditioning protocol in which flies learn to associate an odorant and a concomitant electric shock. Other protocols exist, which exploit aversive visual learning in Drosophila but they require a technology that is not accessible to most laboratories. Thus, the generality of aversive learning mechanisms described so far for olfactory learning in Drosophila remains to be determined. In that sense, an integrative, across-species study on aversive learning is of fundamental importance to uncover the extent to which behavioral, neural and molecular mechanisms of aversive learning are general beyond species-specific, ecological and behavioral contexts. Exploring aversive learning in fruit flies and honeybees is feasible. In particular, it is possible to achieve a multi-level analysis in which behavioral strategies underlying aversive learning are explored in an ecological context, in parallel to the study of both the neural networks, neurotransmitters and molecular signaling cascades responsible for aversive stimulus representation. Our proposal articulates on such a multi-level analysis and constitutes an integrative, comparative study of aversive learning in insects. We will focus on two insects which are well-established models for the study of learning and memory, the fruit fly Drosophila melanogaster, and the honeybee Apis mellifera. In drosophila, aversive learning in a reproductive context and in an appetitive context of food search will be studied. In the honeybee, aversive learning in a defensive context will be investigated. We will characterize aversive memory as arising from these situations and establish a protocol for appetitive malaise common to both bees and flies. We will determine whether or not common neural pathways and mechanisms underlie aversive reinforcement representation despite dissimilarity in learning contexts. We will test the hypothesis that dopaminergic neurons mediate aversive reinforcement independently of the behavioral and ecological context considered. We benefit from a multidisciplinary team in which behavioral, neural, molecular and ecological perspectives will provide a comprehensive view on insect aversive learning, thus affording concrete knowledge to rational management of insect pests and agricultural resources.