Multiple scales of coordination along the body axis during Drosophila 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 towards 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. SIGNIFICANCE STATEMENTMost animals move through the world by coordinating muscle contractions across the bodys many segments. Studying how segments are coordinated in limbless animals can uncover principles that are fundamental for movement across the animal kingdom. However, in one of the best genetic model organisms to address this question, the larval fruit fly, it was unknown how the nearly identical body segments are coordinated across the body. We used machine vision techniques to discover an unanticipated degree of heterogeneity: the timings of muscle activity and movements are more coordinated among tail-end than head-end segments. This provides new insights into animal movements, and opens opportunities to study how interactions of the body and nervous system coordinate segmental movements across an entire animal.