The two-body problem: Proprioception and motor control across the metamorphic divide

Like a rocket being propelled into space, evolution has engineered flies to launch into adulthood via multiple stages. Flies develop and deploy two distinct bodies, linked by the transformative process of metamorphosis. The fly larva is a soft hydraulic tube that can crawl to find food and avoid predators. The adult fly has a stiff exoskeleton with articulated limbs that enable long-distance navigation and rich social interactions. Because the larval and adult forms are so distinct in structure, they require distinct strategies for sensing and moving the body. The metamorphic divide thus presents an opportunity for comparative analysis of neural circuits. Here, we review recent progress toward understanding the neural mechanisms of proprioception and motor control in larval and adult Drosophila. We highlight commonalities that point toward general principles of sensorimotor control and differences that may reflect unique constraints imposed by biomechanics. Finally, we discuss emerging opportunities for comparative analysis of neural circuit architecture in the fly and other animal species.