Disproportionate Cochlear Length in Genus Homo Shows a High Phylogenetic Signal during Apes’ Hearing Evolution

Abstract

Changes in lifestyles and body weight affected mammal life-history evolution but little is known about how they shaped species’ sensory systems. Since auditory sensitivity impacts communication tasks and environmental acoustic awareness, it may have represented a deciding factor during mammal evolution, including apes. Here, we statistically measure the influence of phylogeny and allometry on the variation of five cochlear morphological features associated with hearing capacities across 22 living and 5 fossil catarrhine species. We find high phylogenetic signals for absolute and relative cochlear length only. Comparisons between fossil cochleae and reconstructed ape ancestral morphotypes show that Australopithecus absolute and relative cochlear lengths are explicable by phylogeny and concordant with the hypothetized ((Pan,Homo),Gorilla) and (Pan,Homo) most recent common ancestors. Conversely, deviations of the Paranthropus oval window area from these most recent common ancestors are not explicable by phylogeny and body weight alone, but suggest instead rapid evolutionary changes (directional selection) of its hearing organ. Premodern (Homo erectus) and modern human cochleae set apart from living non-human catarrhines and australopiths. They show cochlear relative lengths and oval window areas larger than expected for their body mass, two features corresponding to increased low-frequency sensitivity more recent than 2 million years ago. The uniqueness of the “hypertrophied” cochlea in the genus Homo (as opposed to the australopiths) and the significantly high phylogenetic signal of this organ among apes indicate its usefulness to identify homologies and monophyletic groups in the hominid fossil record.

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

“…Using the same phylogenetic generalized least squares regression methods and software as in other analyses of this study, we found that the area of the stapes footplate (as a proxy for the potential area of the obturator foramen that passes the stapedial artery) does indeed scale with strong negative allometry to both body mass and endocranial volume: 0.30e0.31, respectively (where isometry would be 0.66) (SOM Part VI). Assuming that footplate area and oval window area are strongly correlated, our results on footplate area can be considered as a confirmation of results for oval window scaling relative to body mass in Braga et al (2015). Braga et al (2015) found an exponent from 0.236 to 0.338 depending on sample composition (see SOM Table S5 of Braga et al, 2015).…”

“…Assuming that footplate area and oval window area are strongly correlated, our results on footplate area can be considered as a confirmation of results for oval window scaling relative to body mass in Braga et al (2015). Braga et al (2015) found an exponent from 0.236 to 0.338 depending on sample composition (see SOM Table S5 of Braga et al, 2015).…”

“…We presume that this negative allometry exists because of a similar negative allometry between the size of the organs of hearing and body mass (Braga et al, 2015 show an exponent of 0.111 between cochlear length and body mass). 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.…”

“…While allometric exponents of ossicular elements are not available for broad comparative samples, Braga et al (2015) show that the area of the oval window (that tightly fits the stapes footplate) scales with an exponent of 0.330 to body mass for catarrhine primates. For their sample of 'non-catarrhine mammals' the exponent is even lower at 0.267 (Braga et al 2015: their figure 6). These relationships suggest strong negative allometry, as an isometric slope of an area to volume is 0.666.…”

“…Under this scenario, as lineages evolve larger body sizes, the stapes will increasingly impinge on blood flow requirements, which e all else being equal e appear to require that canal cross sectional area scales with positive allometry to body mass (Holt et al, 1981;Schmidt-Nielsen, 1984;Sutera, 1993;Dawson, 2014). While allometric exponents of ossicular elements are not available for broad comparative samples, Braga et al (2015) show that the area of the oval window (that tightly fits the stapes footplate) scales with an exponent of 0.330 to body mass for catarrhine primates. For their sample of 'non-catarrhine mammals' the exponent is even lower at 0.267 (Braga et al 2015: their figure 6).…”