Changes in circuit motif during evolution of a species-specific behavior.

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Evolution has generated an enormous variety of morphological, physiological, and behavioral traits in animals. Decades of research have shown that variation in the regulatory regions of particular genes is associated with species differences in morphology (e.g., wing pattern). But how do behaviors evolve in different directions in species equipped with similar neurons and molecular components? Solving these mysteries requires an understanding of the relationship between evolutionarily adaptive changes in behavior and structural/functional changes in neural circuits.******Fruit fly (Drosophila) larvae are useful for this purpose because 1) the Drosophila genus consists of many closely related species that exhibit a wide range of behaviors; 2) they are small enough to generate electron microscope images of the entire nervous system; and 3) the genetic tools and high-throughput behavior analysis techniques available for D. melanogaster make it possible to manipulate single neuron types to understand their function(s) in neural circuits and behavior.******Escape behaviors, which likely evolved under intense evolutionary pressures given their importance for survival, offer a particularly good opportunity to understand behavioral evolution. D. melanogaster larvae roll when attacked by a parasitic wasp. In the laboratory, a nociceptive stimulus triggers rolling. The core circuitry underlying this behavior has recently been mapped out. Preliminary data also show that the probability of rolling varies widely across several closely related Drosophila species. This sets the stage for an exploratory analysis of the neural changes associated with changes in a specific behavior.******This proposal will identify the synapse- and circuit-level changes in structure/function that underlie the divergence of rolling probability in a well-defined sensorimotor circuit. Aim 1 will compare larval escape behaviors in detail across different Drosophila species. Aim 2 will reconstruct the circuitry underlying rolling, with physiological imaging experiments to test for correlations among circuitry, physiology, and behavior. The results should reveal circuit motifs required for adjusting rolling probability, and how variation in the structural/functional properties of circuitry contributes to behavioral evolution in general. ******Our long-term goal is to understand how changes in these features transform behavior at the circuit, cellular, and molecular levels. Such an achievement would constitute one of the first demonstrations of what the renowned sociobiologist E. O. Wilson called consilience—an understanding of behavioral evolution that integrates knowledge vertically across multiple levels of analysis, from molecules at the bottom, to behavior at the top.