Inner Ear Evolution in Primates Through the Cenozoic: Implications for the Evolution of Hearing

Abstract

Mammals are unique in being the only group of amniotes that can hear sounds in the upper frequency range (>12 kHz), yet details about the evolutionary development of hearing patterns remain poorly understood. In this study, we used high resolution X-ray computed tomography to investigate several functionally relevant auditory structures of the inner ear in a sample of 21 fossil primate species (60 Ma to recent times) and 25 species of living euarchontans (primates, tree shrews, and flying lemurs). The structures examined include the length of the cochlea, development of bony spiral lamina and area of the oval window (or stapedial footplate when present). Using these measurements we predicted aspects of low-frequency and high-frequency sensitivity and show that hearing patterns in primates likely evolved in several stages through the first half of the Cenozoic. These results provide temporal boundaries for the development of hearing patterns in extant lineages and strongly suggest that the ancestral euarchontan hearing pattern was characterized by good high-frequency hearing but relatively poor low-frequency sensitivity. They also show that haplorhines are unique among primates (extant or extinct) in having relatively longer cochleae and increased low-frequency sensitivity. We combined these results with additional, older paleontological evidence to put these findings in a broader evolutionary context.