The evolution of embodied postural dynamics underlies behavioral diversity in benthic sessile chordate

Abstract

Benthic animals live on or in the seafloor, a habitat known as the benthic zone. These bottom-dwelling organisms account for the largest fraction of animal diversity in our seas, playing vital roles in nutrient cycling, sediment stabilization and the broader food webs. Historically, the behavioral repertoire of benthic animals attached permanently to the sea floor has been considered as extremely limited (if at all present), reflecting an evolutionary adaptation to their sessile lifestyle and simplified nervous systems. Here, we overturn this view by studying the spontaneous and stimulus evoked behavioral repertoire of the basal chordate Ciona intestinalis which has a benthic sessile adult stage. We found that Ciona adults transition between three main postural engagement behavioral states. These are defined by different body part kinematics and postural dynamics characterised by changes in body shape configuration as opposed to locomotion. Transitions between states can occur probabilistically in spontaneously behaving animals suggesting that they can be internally generated by the simple brain of an adult Ciona. Importantly, using spatiotemporal embedding of postural features, we constructed a behavioral space for Ciona adults, which was divided into 18 stereotyped behavioral modes revealing the unappreciated richness of adult Ciona behaviors. Our analysis showed that Ciona adults can deploy in a selective manner these behavioral modules to elicit distinct responses to different mechanical stimuli, suggesting the presence of a sensory context dependent regulation of behavior in these benthic organisms. Our study raises the possibility that embodied postures is underlie the evolution of behavioral repertoires in sessile benthic animals.