Independent origins of a novel atympanic middle ear system within Chamaeleonidae

Abstract

The evolution of the vertebrate ear is a complicated story of convergence, cooption, loss of function, and occasional regaining of said function. An incredible variety of structures has been adopted as sound receptors, but only chameleons are known to have a bony airborne sound receiver. In some chameleons, the pterygoid bone captures sound vibrations and relays them to the inner ear via a connection to the extracolumella. The distribution of this unique hearing system has not been examined across Chamaeleonidae. Here, I report on dissections on 12 species across four genera and describe their middle ear anatomy for the first time. Half of these species were found to have a link between their extracolumella and pterygoid, and ancestral state reconstruction supports four independent acquisitions of this novel sound-conduction pathway. Species with this pathway tend to have a gular pouch, which seems to produce biotremors and possibly airborne sound, suggesting that this hearing system plays some role in intraspecific communication. Three species were also μ-CT scanned using enhanced contrast to investigate differences in the musculature surrounding the middle ear cavity. In species with a middle ear connected to the pterygoid, the muscles directly lateral to the pterygoid insert farther anterior onto the mandible, which may serve to minimize dampening of vibrations on the pterygoid. Together, these data suggest that the ear plays a more significant role in the lives of some chameleons than has been recognized, and that parallelism is common in the evolution of the ear.