Evolution of Diversity in the Auditory Papillae of Reptiles

Abstract

The independent origins of middle ears in testudinates, lepidosaurs, and archosaurs in the Triassic led to lineage-specific developments in their auditory epithelia. In comparison to the inferred ancestral state, little changed in testudinates, but archosaurs and most lepidosaurs evolved longer, differentiated auditory papillae. In archosaurs, sensory hair cells specialized across and along the papillae, resulting in mainly sensory tall hair cells and mainly mechanically active short hair cells. Crocodilians have 5 mm-long papillae, but relatively low upper frequency limits at around 4 kHz. Avian papillae are mostly 3 to 5 mm in length, being shorter in small species; in owls they exceptionally reach almost 12 mm and have an upper limit of above 10 kHz. Lepidosaurs retained the ancestral papilla as a low-frequency responsive area with one type of hair cell, but most added newly evolved areas (of max. 2 mm length) consisting of oppositely oriented hair cells responding to frequencies above 1 kHz. Initially, these areas flanked both ends of the ancestral area and were redundant in their responses to sound. The evolution of specific configurations in most families eliminated this redundancy, but the paths taken resulted in diverse anatomies that show high degrees of family specificity. Despite these differences, the high-frequency hearing limit of lepidosaurs rarely exceeds 5 kHz.