Role of wing chemosensors in fly orientation behavior – GUSTAILE2011

We are testing 3 Drosophila species and several Drosophila melanogaster populations with diverging geographical distribution and chemosensory-induced behaviors. We will use behavioral, physiological, surgical, genetic and modelization methods to measure the fly response to pheromone and simple food odors in space with one dimension (contention cell), two dimensions (planar chamber) and three dimensions ((flight tunel).

We have already measured the response of flies of wild-type strains and of wing-genetically manipulated strains in the Drosophila melanogaster species, using our 3 dimensions devices. We also measured the variation of biochemical factors (Calcium, cyclicAMP) in the wing of wild-type and mutant flies exposed to different food chemicals.

This new knowledge should help us to rapidly design new strategies (pesticicide-free) compatible with current ecological regulations in order to monitor and eventuallay control populations of pest insects either transmitting human-related diseases (malaria, chikungunia, sleeping sickness) or those involved in the pollinization of flower plants (bees, bumblebess) and those causing agricultural damages (corn borer, ..)

A paper in revision will be shortly resubmitted to a generalist journal (Nature Scientific Reports). The resultas already obtained have been presented as a plenary talk in a european conference (European Conference of Drosophila Neurobiology) in September 2012.

In varied animals (birds, bats, insects), wings provide both lift and propulsion. Flying is useful for many functions: to escape from ground predators, and predate other animals, to explore new ecological niches and find new food source inaccessible to terrestrial animals, to increase the size of the territory and the dispersion of a population, to migrate and find more favorable conditions. Among the 240 000 species of Diptera (insects with one pair of wings), many are important for their contribution on both ecological perspective (pollinization, parasitism) as well as human health (disease transmission). When they fly, flies have to face atmospheric turbulence and wind blow which heavely impact on the dispersion of molecular cues and vortex gradients of odorants, rendering it difficult to trace the emitting source. Apart flight orientation, fly wings may have other roles related to sensory communication like taste, tactile perception, proprioception, and sound production during courtship. Moreover, before or during courtship, flies often brush wings, head and superficial part of the cuticle with the frontal legs. This grooming behavior could serve for chemical self-sampling. If the role of chemosensory hairs present on the antennal, labial, tarsal, maxillary palps appendages and on the female ovipositor have been largely explored this is not the case for the chemosensory hairs carried by the anterior margin of the wing. There is no information for any fly, or insect, on the role that wing sensory organs could play on chemically-driven orientation behaviors. We recently detected the presence of gustatory receptors in wings of aphid, honey bee and in Drosophila. We also found that the partial or total uni- and bilateral wing ablation strongly altered the orientation of Drosophila melanogaster flies to chemosensory cues from a food source or from conspecifics (pheromones). These data taken with the presence of several odorant-binding proteins (OBPs) and some putative odorant receptors in the developing wing. strongly suggest that Drosophila flies use their wings for chemoperception.

Our project will consist to show that Drosophila flies use their wing sensors to orient towards chemical cues. Three Drosophila species will be tested in the three dimensions of space to elucidate the role of wings in chemoperception. We have chosen two cosmopolitan phylogenetically distant species, D.melanogaster, D.virilis, together with D.sechellia, a species closely related to D.melanogaster but with a different chemosensory preference. We will combine behavioral, physiological, surgical, genetic and modelization approaches to reveal the role of wing chemosensors to simple food molecules and to pheromones. Individual flies will be placed either in a small constraining chamber (1-D; autoperception), or in a larger flat chamber (2-D; courtship and guidance in a planar environment), or in a real volume (3-D; orientation in a flight tunnel).

Members of the two teams involved in the project do possess complementary skills and expertise to successfully carry out the different methodological aspects of this project (genetics, wing surgery, electrophysiology, tracking behavior): They have already published results obtained with these methods in international papers. If the two PIs involved in this project have never published together, they have regularly exchanged scientific information for the last 20 years. Moreover, all tools, species and strains required for this project already exist in our labs or are easily available. Therefore, we believe that we can show how the wing neurosensory system is crucial for insects to navigate and investigate their environment. If this will help to monitor insects population in agricultural and urban space, this should also provide new hints to promote alternative tools to neurotoxic pesticides in order to control insect dispersion and proliferation.