Evolution of the Jaw Joint and Middle Ear Morphologies in the Lineage Towards Birds.

Abstract

In tetrapod evolution, the middle ear evolved independently at least four times and represents key innovations for airborne hearing. As the tympanic membrane developed at the interface between the mandibular and hyoid arches, the evolution of middle ears likely involved modifications of jaw joint morphologies. The caudal end of the lower jaw in extant birds accompanies the medial and caudal processes, while the other extant diapsids possess a single process, namely the retroarticular process (RAP). The evolutionary process of these skeletal morphologies, however, remained unclear. Here we examined embryonic developments of the chicken, American alligator, and Chinese soft-shelled turtle, as well as the fossil record, to show that the medial process of the birds is homologous with the retroarticular process. During embryonic development of the chicken, the caudal end of the developing lower jaw became shifted medially, and subsequently the caudal process was secondarily formed. This fact together with the fossil data of Mesozoic theropods indicates that the medial process of the avian lower jaw would be homologous with the RAP. Based on our observations, the invagination of the external auditory meatus likely involves the infolding of the hyoid arch elements including the RAP. Considering the medially oriented RAP as an osteological correlate of the deep external auditory meatus seen in the extant birds, the deep ear canal can be traced back to the common ancestor of coelurosaurian dinosaurs.