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.2015 Jun 17;10(6):e0127780.
doi: 10.1371/journal.pone.0127780. eCollection 2015.

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

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

J Braga et al. PLoS One..

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.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Illustrations of the five cochlear features investigated in this study and expressed as continuous variables.
The external cochlear length (ECL, in mm), number of turns (TUR, expressed as the sum of full circle rotations and the angle between lines “AB”—center to apex—and “AC”—center to base), and relative length (RECL = ECL/TUR, in mm), the curvature gradient (CUR, expressed as a dimensionless ratio between the radii of the larger first—noted “R2”—and the smaller last spiral turns—noted “R1”), and the oval window area (OWA in mm2).
Fig 2
Fig 2. Factorial analysis of all five cochlear features illustrated in Fig 1 and principal component analysis of only RECL, CUR and OWA (to prevent redundancy) measured among hominoid living species and fossil taxa.
Fig 3
Fig 3. Micro-ct values of ECL (in mm) (A), RECL (in mm) (B) and TUR (C) among hominoid living species and fossil taxa.
Summary statistics include sample size (n), the median (bold trait), the 0.25 and 0.75 quartiles, the maximum and minimum values. (D) Bivariate non phylogenetic interindividual linear regressions between ECL and TUR in hominids (filled red circles, n = 53), hylobatids (filled green circles, n = 5) and cercopithecoids (filled blue circles, n = 28) (S4 and S5 Tables). Significant correlation is indicated by * (P≤0.05).
Fig 4
Fig 4. Micro-ct values of OWA (in mm2) (A) and CUR (B) among hominoid living species and fossil taxa.
Summary statistics include sample size (n), the median (bold trait), the 0.25 and 0.75 quartiles, the maximum and minimum values. Bivariate non phylogenetic interindividual linear regressions between RECL and OWA (C), between TUR and CUR (D) in hominids (filled red circles, n = 53), hylobatids (filled green circles, n = 5) and cercopithecoids (filled blue circles, n = 28) (S4 and S5 Tables); Values for the OWA in Neanderthals were taken in Martinezet al. (2004) (S1 Table). Significant correlation is indicated by * (P≤0.05).
Fig 5
Fig 5. Bivariate non phylogenetic and phylogenetically controlled interspecies linear regressions between RECL, OWA and body mass.
(A) RECL (in blue) versus body mass for hominoids (filled circles, n = 9 species mean values), cercopithecoids (open circles, n = 13 species mean values) and non-catarrhine mammal species mean values (black circles, 6 non-catarrhine primate species and 11 non-primate mammal species) (S4 and S5 Tables); dotted lines indicate 95% confidence regions for both the ordinary least squares (OLS) and the phylogenetically controlled regressions. (B) Plots of RECL standardized residuals (y-axis) against RECL standardized predicted values (x-axis) (S1 Text). (C). Histogram of RECL standardized residuals (S1 Text). (D) RECL probability-probability plots (S1 Text). (E) OWA (in red) versus body mass; symbols as in A (filled black circles represent mean values for 25 non-catarrhine primate species). (F,G,H) Residual plots as in (B,C,D). Both non phylogenetic and phylogenetically controlled regressions indicate that only increases of RECL (but not OWA) are the allometric correlates of body mass (which explains 79 to 83% and 70 to 81% of cochlear variation among catarrhine or non-catarrhine primate species). Significant correlation is indicated by * (P≤0.05).
Fig 6
Fig 6. Posterior distributions of ancestral states (S1 Text, S7 Table) for OWA (in red) and RECL (in blue) at each internal node of the hominoid gene-based phylogenetic tree (show in the center).
The hominoid most recent common ancestor is not represented. The ancestral reconstructions are compared with the actual mean values obtained through micro-ct measurements on the fossilOreopithecus bambolii,Australopithecus sp.,Paranthropus robustus,Homo erectus and Neanderthals. Significant deviations of each fossil value from each posterior distribution is calculated with Z-scores (S7 Table) and indicated by * (P≤0.05).
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