Coordinated transformations of the labyrinth and occiput during the dinosaur-bird transition

Evolutionary shape changes of the vertebrate semicircular canals (SCCs) are often ascribed to evolutionary transitions in locomotion, including the origin of flight during the dinosaur-bird transition. However, the potential for transformations of braincase architecture to influence SCC shape independent of sensory-functional adaptation has generally been overlooked. We evaluate the influence of both factors using a large dataset of 146 living and recently extinct crown birds, including taxa representing ~24 independent evolutionary losses of flight, together with Mesozoic stem avialans, nonavialan dinosaurs, and pterosaurs. Among crown birds, evolutionary changes in locomotor capabilities, including the total loss of flight, have only weak effects on SCC shape, contrasting with large effects from changes in braincase geometry. Notably, rotation of the occiput toward a ventral orientation is associated with important changes to SCC shape that match those observed during the dinosaur-bird transition. This suggests that evolutionary transformations of SCC shape during the Mesozoic origin of avian flight resulted from evolutionary changes in the orientation of the craniocervical joint, and not from tuning of SCC sensory function. These findings illuminate the importance of integrated morphological changes to the head-neck system during bird origins and challenge the long-standing assumption that SCC morphology enables confident inferences of the locomotor capabilities of extinct vertebrates.