Behavioral ontogeny in a pelagic tunicate reveals the deep origins of chordate behavioral developmental plasticity

ABSTRACT Behavioral developmental plasticity refers to the lasting changes in an organism’s behavior that occur during development in response to external and internal cues, enhancing survival and reproduction. While well studied in vertebrates, its occurrence in other chordates, including tunicates, the closest relatives of vertebrates, remains unclear. We built a behavioral atlas of the planktonic tunicate Oikopleura dioica across its life cyclefrom larval to adult stages using high-throughput tracking and unsupervised analysis. Swimming kinematics, exploration, and thigmotaxis increased with development. Adults exhibit a unique innovation, known as the house, a complex extracellular filtration structure encasing the animal trunk, which drastically alters locomotion and exploration compared to free-swimming individuals. Postural variation during ontogeny is captured by seven basic shapes (“eigenoikopleuras”), with complex shapes becoming more frequent over time. Spatiotemporal embedding and Hidden Markov modeling revealed that behavioral refinement arises from changes in motor modules and their transitions. House occupancy similarly shifts these modules, indicating context-specific specialization. This continuous behavioral maturation parallels Oikopleura ’s neotenic morphology, retaining a larval body plan unlike other tunicates. Our atlas provides a quantitative framework for exploring the evolution of behavioral developmental plasticity in chordates.