The evolution of mechanosensory perception in the context of oviposition site choice in Drosophila
General Genetics and Functional Genome Biology
Molecular Biology and Physiology of Neurons and Glial Cells
Final Report Abstract
Animal diversity is manifest, not only in the seemingly infinite variations of their morphology, but also in the variety of their innate behaviors. Our understanding of behavior evolution, however, remains limited. For this reason, my group uses a simple paradigm to examine the genetic and neuronal changes underlying a simple change in behavior. We study how a female fly choses a suitable site to lay her eggs. This choice is diverse among Drosophila with different ecologies. For instance, the invasive pest species D. suzukii hardly choses between substrates of different stiffness, unless the difference is equivalent to that of a green strawberry vs. a ripe strawberry. By contrast, D. melanogaster proves extremely choosy, and prefers the stiffness equivalent to that of a rotten fruit over that of a very ripe fruit. With this project, we have dissected how a female D. melanogaster fly senses and selects substrate stiffness at the genetic, molecular, and neuronal levels. In brief, we have found that the mechanoreceptor gene painless, a TRP channel expressed in many sensory and central neurons, is directly involved in sensing the texture of a potential oviposition substrate. We established that this choice is mediate by two types of mechanosensory organs of the fly tarsae, ventral mechanosensory bristles and campaniform sensilla located near the tarsal joints. We have shown that blocking neurotransmission specifically in neurons innervating these organs, or depleting painless product from them impairs the ability of flies to choose an appropriate egg-laying substrate. We submit that the perception of substrate stiffness follows two independent sensory pathways. First mechanosensory bristles contact the substrate directly and record its resistance. Second, a fly standing on a substrate will experience an opposing force from the substrate that will vary with the substrate stiffness, much like the opposing force of snow is different from that of concrete. As a result, the tarsus of a fly will bend and campaniform sensilla located at the tarsal joints will record the corresponding compression of the cuticle. We expect the degree of tarsal bending to vary with substrate stiffness, and therefore, the neuronal activity of campaniform sensilla to be different on a soft substrate and on a stiff substrate. Understanding how flies with preferences for different stiffness make their choice is what motivated the dissection of this process. We therefore started to explore how the recording of substrate stiffness may differ in Drosophila suzukii. To this end, we first asked whether there are changes in the function of expression of the mechanoreceptor painless. We also started to develop genetic tools to later characterize and compare neuronal activity in both species, D. melanogaster and D. suzukii. Together, our work revealed an unexpected mechanism for the evaluation of substrate texture, involving cuticle compression, and contrasting with the direct recording of stiffness that had been found in other systems. We are now positioned to unravel evolutionary differences that have led to behavioral diversification.
Publications
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Odor-regulated oviposition behavior in an ecological specialist. Nature Communications, 14(1).
Álvarez-Ocaña, Raquel; Shahandeh, Michael P.; Ray, Vijayaditya; Auer, Thomas O.; Gompel, Nicolas & Benton, Richard
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Painless-mediated stiffness sensing of egg-laying substrates in Drosophila melanogaster. European Drosophila Research Conference, Lyon, France. Poster presentation.
Ray V., Cury K., Kourtidis A., Bracker L.B., Jaenichen R., Muhling B. & Gompel N.
