Flat or flexible? Evolutionary cranial biomechanics and the origins of modern archosaur skulls

Abstract

The divergent specializations of living archosaurs, crocodilians and birds, represent two of the great transformations in vertebrate evolution. Despite hailing from common ancestor with a tall skull, braced palate and relatively unspecialized jaw muscles, these two living clades followed disparate paths in cranial biomechanics and feeding functional morphology during the Mesozoic era, resulting in the flat, rigid skulls in crocodylians and the bulbous and beaked, flexible skulls of birds. Here we use new approaches in imaging, 3D modeling, morphometrics, lever mechanics, finite element modeling and phylogenetic comparative methods of living and extinct reptiles to show how morphological and functional changes in the palate, cranial joints and jaw musculature occurred within the fossil record of these lineages that were key features in acquisition of the modern forms. We show how jaw muscles reoriented their resultants and moments about jaw joints during skull flattening, palatocranial suturing and feeding specializations in Jurassic crocodyliforms. These morphological changes resulted in a decrease in mechanical efficiency of the feeding apparatus that was compensated for by an increase in jaw muscle sizes and canalized muscle architecture. Meanwhile, along the line to living birds, the acquisition of enlarged brains in coelurosaur dinosaurs resulted in a shifting of temporal and palatal muscle positions, a canalization of vertically‐oriented of muscle forces and consequently reorientation of their moments about palatocranial joints. These changes in loading environment, along with a concatenate increase in the propulsive and bending properties of the palate, facilitated cranial kinesis in neoavian birds. Together, these examples of evolutionary innovation in reptile cranial biomechanics reveal powerful new approaches to testing biomechanical and evolutionary hypotheses in any cranial or appendicular musculoskeletal system.