Embryonic origins of the flattened skull table and snout in Crocodylia

Abstract

Major groups of vertebrates, such as mammals, birds, and crocodylians, are recognizably distinct due to unique anatomical, physiological, and behavioral characteristics. The origins and ecological consequences of these features have been the focus of intense research, including more recently the developmental mechanisms facilitating their evolution. The dorsoventrally flattened snout and skull table typify extant Crocodylia perhaps more than any other anatomical feature. The origins and ecological consequences of the crocodylian skull have been the focus of extensive study. While it is generally recognized as an adaptation for feeding at the water's surface, the developmental origins of craniofacial flattening have yet to be explored. To understand how the skull table and platyrostral snout develop, we quantified the embryonic development and post-hatching growth (ontogeny) of the crocodylian skull in lateral view using geometric morphometrics. Our dataset (n=103) includes all but one extant genus and all of the major ecomorph groups, including the rare and extremely slender-snouted Gavialis and Tomistoma. Our ontogenetic morphospace captures similar variation in snout length as have been previously found for the ontogeny of dorsal snout shape, including the presence of a conserved embryonic skull shape for all but the two most extremely slender-snouted forms. Comparisons of ontogenetic trajectories revealed that by the end of embryonic development the adult condition of a dorsally flat skull table is achieved in all species and that ecomorphs did not differ in their pattern of skull roof ontogeny. The ontogenetic flattening of the snout did show post-hatching differences among ecomorphs, likely related to differences in the length and depth of the snout, but not during embryonic development. These anatomical changes correlate with recently described molecular and cellular processes that pattern the temporal and facial form, allowing the identification of developmental mechanisms which potentially facilitated the origin of these apomorphic features. These findings demonstrate that the iconic flattened skull table and platyrostral face of Crocodylia are the result of a conserved pattern of shape changes during embryonic development. Considering that these features appear by the Early Jurassic among extinct stem crocodylians, it is likely that these aspects of cranial development have been conserved for over 200 million years.