Behavioural plasticity in Caenorhabditis elegans navigating dynamic granular environments

The mechanisms that steer behavioural plasticity in complex environments remain poorly understood. Here, we introduce Peb2les, a quasi-two-dimensional granular arena, for the behavioural assessment of Caenorhabditis elegans nematodes, as they interact with deformable, dynamic terrains. Using customized deep-learning-based methods, we track both nematodes and particles to characterize coupled animal-environment dynamics. We find that nematodes locomotor performance depends on particle density and surface properties, and is largely independent of mechanosensation, whereas functional touch sense is required for the initial decision to enter rough-textured arenas. In addition, we identify a previously undescribed touch-seeking behaviour that partially depends on mechanosensation, in which C. elegans actively return to the granular arena after exiting. In parallel, locomoting nematodes rearrange and stack surrounding particles, continuously modifying the granular terrain. Together, these findings establish Peb2les as a versatile platform for probing the mechanism and limits of behavioural plasticity and locomotory adaptability of nematodes in sensory-enriched, soil-like environments, while also providing insight into the potential evolutionary origins of adaptive touch-seeking behaviours in animals.