Abstract
Chemotaxis to a moving potential mate emitting a volatile sex pheromone poses a navigation challenge that requires rapid, precise responses to maximize reproductive success. Volatile chemicals form gradients that differ from soluble compounds, potentially making navigation based on comparisons between spatially separated sensors unreliable for small-bodied animals. Contrary to this model of simple spatial comparison, C. elegans employs an antagonistic strategy, comparing inputs from head (AWA) and tail (PHD) sensory neurons with distinct response properties. Despite sharing a receptor, SRD-1, these detectors play different roles: AWA head neurons promote forward movement and acceleration, while tail PHD neurons induce reversals and deceleration. In increasing pheromone gradients AWA dominates; whereas decreasing gradients inactivate AWAs, allowing PHDs to fine-tune the response and correct the trajectory. Head AWAs are essential for mate-searching, while tail PHDs are crucial for complex tasks. Using a minimal-parameter computational model that recapitulates key findings, we infer the interplay between head and tail signals in adaptive navigation. This study reveals a sexually dimorphic dual-detector system that integrates antagonistic sensory inputs from head and tail neurons to enable adaptive navigation strategies essential for efficient free-moving target location in dynamic environments.