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. Anat Rec,

The nocturnal bottleneck and the evolution of activity patterns in mammals

“…As a result, other senses, including improved olfactory sensitivity [86], high-frequency hearing [87] and the development of tactile vibrissae (whiskers) [88], became more acute.…”

Internal carotid arterial canal size and scaling in Euarchonta: Re-assessing implications for arterial patency and phylogenetic relationships in early fossil primates

“…In other words, we expect the size of middle ear components to covary with that of inner ear structures to a large degree so that the two systems can work as an integrated whole in audition. In turn, the scaling relationship between the organs of hearing and brain/body size seems to be a consequence of the fact that cochlear volume (Kirk and GosselinIldari, 2009) and length (Coleman and Boyer, 2012) are strong determinants of hearing frequency sensitivity. The absolute interspecific variation in size of the hearing organs may therefore be constrained by demands on the auditory system, unlike brain size or body size.…”

The labyrinthine morphology of Pronycticebus gaudryi (Primates, Adapiformes)

“…3). And even though Tarsiers have more spiral turns and have longer cochleae than Omomyids (Coleman and Boyer 2012), they share with small anthropoids some other aspects of morphology of the cochlea: we found that Tarsius, microchoerines and small anthropoids have anteriorly oriented cochleae exhibiting a second turn staying away from the plane of the first turn, and posteriorly oriented common crura. These three characters are candidate synapomorphies for the inner ears of haplorhines.…”

“…Morphological variation of the bony labyrinth across taxa reflects differences in locomotor behavior (Silcox et al 2009;Spoor and Zonneveld 1998;Spoor et al 2007;Walker et al 2008 ) and hearing performance (Coleman and Boyer 2012;Echteler et al 1994;Gleich et al 2005; Kirk and Gosselin-Ildari 2009;West 1985). This structure is thus highly functionally constrained.…”

“…Nevertheless, a part of labyrinthine morphological variation may still convey phylogenetic information. Basilar membrane length, the number of spiral turns and cochlear volume relate to low frequency and high frequency sensitivity (Coleman and Boyer 2012;Echteler et al 1994;Kirk and Gosselin-Ildari 2009;West 1985). However, other aspects of the morphology of the cochlea, such as its general geometry and orientation relative to the semi-circular canal system are less likely to reflect hearing performance.…”