Neuromodulation of swarming behavior in <i>Caenorhabditis elegans</i>: Insights into the conserved role of calsyntenins.

Abstract

Collective animal behaviors arise from a complex interplay between internal physiological states and external environmental cues. In <i><i>Caenorhabditis elegans</i></i>, favorable conditions promote dispersal, while stressors like food scarcity trigger aggregation. Here, we describe a distinct self-organized swarming behavior, where <i>C. elegans</i> move and feed in groups driven by uncontrolled local increases in population density despite abundant food availability. While various environmental factors have been implicated in collective behaviors in <i>C. elegans</i>, the underlying genetic and molecular mechanisms remain unclear. We identify a key role for the conserved calsyntenin protein CASY-1 in regulating swarming. Through genetic, behavioral, and optogenetic approaches, we show that CASY-1 functions to modulate the neuropeptide pigment-dispersing factor (PDF) signaling. Mutants in <i>casy-1</i> show impaired PDF-1 signaling and reduced inhibition of the serotonin pathway, a known regulator of social behaviors. This dysregulation, along with its associated mechanosensory and foraging defects, likely contributes to the swarming phenotype. Our findings reveal a putative neuromodulatory pathway critical for swarming behavior in <i>C. elegans</i>.