Tonic immobility in cartilaginous fishes (Chondrichthyes): function, evolutionary history, and future directions

Abstract

Tonic immobility, a temporary cessation of voluntary movements, is a widespread phenomenon within the animal kingdom. While commonly regarded as an ‘anti-predator’ defence strategy, empirical evidence supporting this hypothesis is predominantly limited to terrestrial vertebrates. In Chondrichthyes (i.e., sharks, rays, and chimaeras), tonic immobility has also been proposed as an anti-predator mechanism, despite a dearth of evidence and fundamental physiological distinctions from terrestrial counterparts. Here, we present data regarding tonic immobility induced by dorsoventral inversion across 13 chondrichthyan species. We also perform a review of the existing literature to identify temporal, taxonomic, and methodological trends in TI research. Then, using phylogenetic comparative methods, we demonstrate that this trait is plesiomorphic to Chondrichthyes and has been independently lost multiple times throughout chondrichthyan phylogeny. Contrary to expectations, we find no significant correlation between the evolutionary transitions in tonic immobility and major ecological axes of variation in Chondrichthyes. Our findings challenge existing hypotheses and suggest that tonic immobility may lack adaptive significance in extant chondrichthyans, persisting through chondrichthyan phylogeny due to minimal net fitness costs. Additionally, we propose an association between the loss of tonic immobility and entanglement risk in shallow-water benthic ecosystems. Our results provide unprecedented insights into the evolutionary history of this enigmatic behaviour within Chondrichthyes and across the phylogeny of jawed vertebrates.