Multiple Scales of Coordination along the Body Axis during <i>Drosophila</i> Larval Locomotion

Abstract

Coordinated movement along the body axis is critical to locomotion. In segmented, limbless animals, anterior (head) and posterior (tail) segments play different roles in locomotion, leading to a need for flexible coordination across body regions. Larval Drosophila melanogaster present a tractable experimental model for limbless, segmented crawling given the extensive genetic tools available and the optical clarity of the body. Prior work has suggested that, during crawling, all larval body segments contract similarly, despite the fact that each crawl cycle comprises two overlapping phases: a piston involving the most posterior segments and a peristaltic wave involving all body segments. To test whether coordination varies regionally during locomotion, we expressed GCaMP in body wall muscles of larvae of either sex and recorded segmental contraction kinematics and muscle recruitment during many cycles of locomotion in linear channels. Facilitated by machine vision techniques, we discovered new features of larval crawling at multiple scales. First, the propagation of both contraction and recruitment waves slowed approaching mid-body segments, then sped up toward the head. Second, the timing relationship between contraction and recruitment waves could be highly variable in anterior segments. Third, contraction durations showed particularly strong intersegmental correlations among posterior segments. These data suggest posterior segments coordinate to power the piston phase, while anterior segments tolerate greater flexibility to enable reorienting behaviors. Our results depict an unanticipated degree of axial heterogeneity in the coordination of limbless crawling, opening new avenues to study the origins of whole-body coordination and the consequences of segmental diversity for locomotion.