The cellular basis of locomotor evolution: insights from larval insects

Animals move through their environments using remarkably diverse locomotor behaviors, which are critical for their survival and success. All movement, including locomotion, requires the coordinated function of three components: the central nervous system (CNS), the peripheral nervous system (PNS), and the musculature. Although evolutionary change in any one of these components can alter locomotion, how these changes arise and combine to generate behavioral diversity remains poorly understood. Larval insects are an exceptional system for addressing this question: they combine extensive behavioral and morphological diversity with relatively simple, stereotyped anatomy, enabling cell-level homology inferences and quantitative cross-tissue comparisons. We first review anatomical evidence for the long-standing peripheral change hypothesis, which posits that locomotor diversity is primarily driven by modifications to peripheral structures, such as muscles, while central circuits remain conserved. We then propose an alternative hypothesis, the motor neuron bottleneck hypothesis, which draws on comparative neurodevelopmental data to suggest that motor neurons are disproportionately conserved relative to both upstream sensory neurons and interneurons and downstream muscles. Finally, we consider how connections are maintained between the CNS, PNS, and musculature when these components change in number. Throughout, we assess relative rates of evolutionary change in cell number across nested phylogenetic scales, from the Drosophila genus to the Diptera order to the Holometabola supraorder. By integrating anatomical, developmental, and functional perspectives, larval insects emerge as a powerful comparative model for uncovering general evolutionary principles.