1. Evolutionary Biology

The evolution of the vestibular apparatus in apes and humans

  1. Alessandro Urciuoli  Is a corresponding author
  2. Clément Zanolli
  3. Amélie Beaudet
  4. Jean Dumoncel
  5. Frédéric Santos
  6. Salvador Moyà-Solà
  7. David M Alba  Is a corresponding author
  1. Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain
  2. Laboratoire PACEA, UMR 5199 CNRS, Université de Bordeaux, France
  3. University of the Witwatersrand, South Africa
  4. University of Pretoria, South Africa
  5. Laboratoire AMIS, UMR 5288 CNRS, Université de Toulouse, France
  6. Institució Catalana de Recerca i Estudis Avançats (ICREA), Spain
https://doi.org/10.7554/eLife.51261
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Cite this article
  1. Alessandro Urciuoli
  2. Clément Zanolli
  3. Amélie Beaudet
  4. Jean Dumoncel
  5. Frédéric Santos
  6. Salvador Moyà-Solà
  7. David M Alba
(2020)
The evolution of the vestibular apparatus in apes and humans
eLife 9:e51261.
https://doi.org/10.7554/eLife.51261
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13 figures, 9 tables and 2 additional files

Figures

Figure 1
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The vestibular apparatus of extant hominoids, other anthropoids, and some fossil hominoids, in lateral view.

(a) Homo sapiens (EMBR 121); (b) Pan paniscus (MCZ 38019); (c) Pan troglodytes (AMNH.M 51204); (d) Gorilla gorilla (AMNH.M 167338); (e) Pongo pygmaeus (IPS 10647); (f) Hylobates lar (MCZ 41424); (g) …

Figure 2 with 1 supplement
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Main patterns of vestibular shape variation among the analyzed anthropoid sample as shown by bivariate plots of principal components from the between-group principal components analysis (bgPCA) using a few major clades (i.e., platyrrhines, cercopithecoids, hylobatids and hominids) as grouping factor.

(a) bgPC2 vs. bgPC1. (b) bgPC3 vs. bgPC1. Variance explained by each bgPC is included within parentheses. Color code: dark green, platyrrhines; orange, hominids; red, hylobatids; brown, papionins; …

Figure 2—source data 1

Individual scores for all the principal components (bgPC) yielded by the between-group principal components analysis (bgPCA) of deformation-based 3DGM of vestibular shape for anthropoids, using major taxa (i.e., hominids, hylobatids, cercopithecoids, and platyrrhines) as grouping factor.

The variance explained by each bgPC is reported within parentheses. Table provided as a separate Excel file.

https://cdn.elifesciences.org/articles/51261/elife-51261-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
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Box-and-whisker plots of the principal components (bgPCs) from the between-group principal components analyses (bgPCA) of vestibular shape for the anthropoid sample.

(a) bgPC1; (b) bgPC2; (c) bgPC3. Colored stars correspond to: green, Oreopithecus; black, Australopithecus sp. (StW 573); red Australopithecus sp. (StW 578).

Figure 3
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Results of the 3DGM deformation-based analysis superimposed on the vestibular apparatus of hominoids in lateral view.

Cumulative displacement variations are rendered by pseudocolor scale ranging from dark blue (5.1 µm) to dark red (0.42 mm). Black arrows correspond to the vectors identifying the direction and …

Figure 4
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Results of the 3DGM deformation-based analysis superimposed on the vestibular apparatus of hominoids, in superior view.

Cumulative displacement variations are rendered by pseudocolor scale ranging from dark blue (<5.1 µm) to dark red (0.42 mm). Black arrows correspond to the vectors identifying the direction and amoun…

Figure 5
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Results of the 3DGM deformation-based analysis superimposed on the vestibular apparatus of hominoids in posterior view.

Cumulative displacement variations are rendered by pseudocolor scale ranging from dark blue (<5.1 µm) to dark red (0.42 mm). Black arrows correspond to the vectors identifying the direction and amoun…

Figure 6
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Results of the 3DGM deformation-based analysis superimposed on the vestibular apparatus of the fossil specimens included in the present study.

Each vestibule is displayed in lateral (left), superior (middle), and posterior (right) views. Cumulative displacement variations are rendered by pseudocolor scale ranging from dark blue (<5.1 µm) …

Figure 7
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Bivariate regressions between (a) vestibular shape (as represented by bgPC1) and log-transformed cube root of vestibular volume (ln Vol), and (b) semicircular canal log-transformed cube root of volume (ln VolSC) vs.log-transformed length (ln L).

Lines represent OLS best-fit lines for the whole anthropoid sample (black), hominids (red), and other anthropoid taxa (blue). Note that there is a significant correlation between bgPC1 (which …

Figure 7—source data 1

Linear measurements for the analyzed specimens and used for computing the linear regressions.

Table provided as a separate Excel file.

https://cdn.elifesciences.org/articles/51261/elife-51261-fig7-data1-v1.xlsx
Figure 8
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Tangent space of vestibular shape among the analyzed anthropoid sample as shown by bivariate plots of principal components from the PCA of deformation-based analysis.

Variance explained by each PC is included within parentheses. Convex hulls correspond to: hominids (orange), hylobatids (red), cercopithecoids (blue), platyrrhines (green). Color code: dark green, …

Figure 8—source data 1

Individual scores for all the principal components (PC) yielded by the principal components analysis (PCA) of deformation-based 3DGM of vestibular shape for anthropoids.

The variance explained by each PC is reported. Table provided as a separate Excel file.

https://cdn.elifesciences.org/articles/51261/elife-51261-fig8-data1-v1.xlsx
Figure 9
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Main patterns of vestibular shape variation among the analyzed anthropoid sample as shown by bivariate plots of principal components from the landmark-based between-group principal components analysis (bgPCA) using major taxa as in Figure 2.

(a) bgPC2 vs. bgPC1. (b) bgPC3 vs. bgPC1. Variance explained by each bgPC is included within parentheses. Lateral (top), superior (middle), and anterior (bottom) views of landmarks and semilandmark …

Figure 9—source data 1

Individual scores for all the principal components (bgPC) yielded by the between-group principal components analysis (bgPCA) of landmark-based 3DGM of vestibular shape for anthropoids, using major taxa (i.e., hominids, hylobatids, cercopithecoids, and platyrrhines) as grouping factor.

The variance explained by each bgPC is reported within parentheses. Table provided as a separate Excel file.

https://cdn.elifesciences.org/articles/51261/elife-51261-fig9-data1-v1.xlsx
Figure 10
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Reconstructed evolutionary history of the vestibular apparatus in the sample restricted to hominoids.

The depicted phylomorphospaces are obtained by projecting the phylogeny displayed in Figure 13 on the bivariate plots between principal components: (a) bgPC2 vs. bgPC1 (see Figure 2a); (b) bgPC3 vs. …

Figure 11
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Reconstructed vestibular shape for the last common ancestors (LCA) of the main clades of interest as reconstructed using maximum likelihood methods for deformation-based 3DGM analyses applied to the anthropoid sample (Figure 7), in lateral (left), superior (middle), and posterior (right) views.

Cumulative displacement variations are rendered by pseudocolor scale ranging from dark blue (<5.1 µm) to dark red (0.42 mm). Black arrows correspond to the vectors identifying the direction of …

Figure 12
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Illustration of hominoid, hominid and hylobatid synapormophies for the vestibular apparatus.

See Table 8 for further details. character #1: (a) rounded (gray) and compressed (green) anterior canal; character #2: (b–c) non-posteriorly displaced posterior canal (gray), posteriorly displaced …

Figure 13
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Time-calibrated molecular phylogeny of extant anthropoids used in the analyses of phylogenetic signal and PGLS regressions as inferred from a species supermatrix.

Fossil taxa have been added a posteriori according to their phylogenetic position and their point estimates correspond to their last occurrence in the fossil record (Rook et al., 2000; Wood and …

Tables

Table 1
Percentage of correctly classified individuals with cross-validation according to the groups (hominids, hylobatids, cercopithecoids, platyrrhines) used in the between-group principal components analysis based on group-centroid distances.
CercopithecoideaHominidaeHylobatidaePlatyrrhini
Cercopithecoidea96.3%3.8%0.0%0.0%
Hominidae3.3%96.7%0.0%0.0%
Hylobatidae5.9%0.0%94.1%0.0%
Platyrrhini0.0%0.0%0.0%100.0%
Table 2
Phylogenetic signal results for a between-group principal components analysis (bgPCA) applied to vestibular shape deformation fields in the analyzed sample of extant anthropoids.
bgPC1bgPC2bgPC3
Variance68.79%19.60%11.61%
Eigenvalue0.8210.2340.138
Pagel’s λ1.000 (p<0.001)0.921 (p<0.001)1.000 (p<0.001)
Blomberg’s K1.152 (p<0.001)1.514 (p<0.001)1.163 (p<0.001)
Table 3
Posterior probabilities of group membership based on the bgPC scores for fossil specimens in the analysis based on the anthropoid sample.

Note that these are probability estimates of having a particular score given membership in a particular group, not the likelihood of group membership in each of a priori defined groups given a …

CercopithecoideaHominidaeHylobatidaePlatyrrhini
BAC 208 (Oreopithecus)p=0.046p=0.013p<0.001p=0.012
StW 573 (Australopithecus)p=0.005p=0.678p<0.001p<0.001
StW 578 (Australopithecus)p<0.001p=0.190p<0.001p<0.001
Table 4
Posterior probabilities of group membership based on the bgPC scores for fossil specimens in the analysis restricted to hominoid genera.

Note that these are probability estimates of having a particular score given membership in a particular group, not the likelihood of group membership in each of a priori defined groups given a …

HoolockHylobatesSymphalangusPongoGorillaPanHomo
BAC 208 (Oreopithecus)p<0.001p<0.001p<0.001p<0.001p<0.001p=0.002p=0.026
StW 573 (Australopithecus)p<0.001p<0.001p<0.001p=0.019p<0.001p=0.368p=0.264
StW 578 (Australopithecus)p<0.001p<0.001p<0.001p=0.062p=0.077p=0.030p=0.727
Table 5
Bivariate regressions of vestibular shape vs. volume and of semicular canal volume vs. length.

Both ordinary least-square linear regressions (OLS) and phylogenetic generalized least-square regressions (PGLS) are provided for the whole anthropoid sample, as well as hominids and non-hominids …

R2pslopeSE95% CIinterceptSE95% CI
OLS
Anthropoids (n = 142)
 bgPC1 vs. ln Vol0.635<0.0015.2570.3354.6005.914−6.1910.399−6.973−5.409
 bgPC2 vs. ln Vol0.0080.1460.4530.309−0.1541.060−0.5330.368−1.2540.188
 bgPC3 vs. ln Vol0.0000.3850.1920.220−0.2390.622−0.2260.261−0.7380.287
 ln VolSC vs. ln L0.288<0.0010.8970.1180.6661.128−2.3280.429−3.169−1.487
Hominids (n = 30)
 bgPC1 vs. ln Vol0.480<0.0016.4961.2334.0798.913−7.7811.797−11.303−4.259
 bgPC2 vs. ln Vol0.0260.195−1.4001.054−3.4660.6662.3071.538−0.7085.322
 bgPC3 vs. ln Vol0.0390.153−0.7200.490−1.6810.2401.0360.714−0.3652.436
 ln VolSC vs. ln L0.2510.0030.6210.1900.2490.992−1.0840.705−2.4650.297
Non-hominids (n = 112)
 bgPC1 vs. ln Vol0.0580.0061.9900.7090.6013.380−2.6450.785−4.183−1.108
 bgPC2 vs. ln Vol0.0100.152−1.0270.712−2.4220.3681.0610.788−0.4822.605
 bgPC3 vs. ln Vol0.0460.0131.3320.5290.2952.368−1.4660.585−2.613−0.319
 ln VolSC vs. ln L0.219<0.0010.4540.0800.2970.611−0.7830.291−1.352−0.213
PGLS
Anthropoids (n = 27)
 bgPC1 vs. ln Vol0.2610.0043.4011.0651.3145.488−3.7191.376−6.416−1.022
 bgPC2 vs. ln Vol0.0030.4160.6250.756−0.8582.107−1.270.962−3.1550.615
 bgPC3 vs. ln Vol0.0630.111−0.7270.440−1.5890.1350.8790.570−0.2381.996
 ln VolSC vs. ln L0.437<0.0010.5020.1090.2880.7163.1440.1242.9013.388
Hominids (n = 5)
 bgPC1 vs. ln Vol0.2210.2404.4403.042−1.52110.402−4.6274.499−13.4454.192
 bgPC2 vs. ln Vol0.0360.760−1.1443.421−7.8505.5611.8924.990−7.88811.672
 bgPC3 vs. ln Vol0.0620.687−0.3920.883−2.1221.3380.5961.309−1.9703.162
 ln VolSC vs. ln L0.5530.0930.6310.2590.1241.1382.9200.3272.2793.561
Non-hominids (n = 22)
 bgPC1 vs. ln Vol0.0080.2941.3761.276−1.1253.877−1.6741.512−4.6391.290
 bgPC2 vs. ln Vol0.0300.4450.7630.978−1.1542.679−1.4441.152−3.7010.814
 bgPC3 vs. ln Vol0.0200.500−0.4190.610−1.6160.7770.5770.730−0.8542.008
 ln VolSC vs. ln L0.504<0.0010.6340.1340.3710.8963.0520.1372.7843.320
Table 6
Probability of correct classification of individuals from the hierarchical clustering analyses of deformation fields according to the groups (hominids, hylobatids, cercopithecoids, platyrrhines) used in the bgPCA.
HominidaeHylobatidaeCercopithecoidaePlatyrrhini
90.0%23.5%65.0%66.7%
Table 7
Phylogenetic signal results for a between-group principal components analysis (bgPCA) applied to vestibular shape procrustes residuals in the analyzed sample of extant anthropoids.
bgPC1bgPC2bgPC3
Variance53.34%29.29%17.37%
Eigenvalue2.4621.3520.802
Pagel’s λ1.000 (p<0.001)0.902 (p<0.001)0.932 (p=0.006)
Blomberg’s K1.226 (p=0.001)1.081 (p=0.001)0.528 (p=0.01)
Table 8
Phylogenetically informative discrete characters of vestibular morphology that represent potential synapomorphies of either hominoids or hominids.
Character #Character definitionCharacter statesaSynapomorphic for
#1Anterior SCb0 = rounded; 1 = vertically compressedHominoidea
#2Posterior SC0 = non posteromedially displaced; 1 = posteromedially displacedHominoidea
#3Insertion of the lateral SC slender portion on the vestibule0 = posterior (lateral SC intersecting the posterior SC plane); 1 = anterior (not intersecting)Hominoidea
#4Lateral SC medial portion0 = curved; 1 = straightHominoidea
#5Trajectory of the lateral SC ampullar portion0 = flat; 1 = bent upwardsHominoidea
#6Angle between the planes identified by the anterior and posterior SCs0 = close to right angle, 1 = obtuseHylobatidae
#7Inclination and size of the posterior SC relative to the size of the anterior and lateral SCs0 = forming a right angle and equal or larger in size, 1 = posteriorly tilted and smallerHylobatidae
#8Robusticity of SCs0 = slender; 1 = stoutHominidae
#9Extension of vestibular recesses relative to that of the SCs0 = smaller; 1 = similar in sizeHominidae

  1. Abbreviations: SC = semicircular canals.

    a Character state 0 represents the primitive condition reconstructed for the last common ancestor of crown catarrhines.

  2. b Some platyrrhines display a superior eccentricity of the anterior SC that might be apomorphic.

Table 9
Sample of extant anthropoid specimens analyzed in this paper based on µCT image stacks.

See Supplementary file 1 for further details on each specimen.

FamilySpeciesnMF?
AtelidaeAlouatta palliata5320
AtelidaeAteles geoffroyi5140
CebidaeCebus apella5320
CercopithecidaeCercocebus galeritus5320
CercopithecidaeCercopithecus mitis5050
CercopithecidaeChlorocebus pygerythrus5230
CercopithecidaeColobus guereza5230
CercopithecidaeErythrocebus patas5320
CercopithecidaeLophocebus albigena5230
CercopithecidaeMacaca fascicularis5140
CercopithecidaeMandrillus sphinx5500
CercopithecidaeMiopithecus talapoin5320
CercopithecidaeNasalis larvatus5050
CercopithecidaePapio anubis5320
CercopithecidaePiliocolobus badius5410
CercopithecidaePresbytis hosei5140
CercopithecidaePresbytis rubicunda5230
CercopithecidaeTheropithecus gelada5410
CercopithecidaeTrachypithecus cristatus5050
HylobatidaeHoolock hoolock6240
HylobatidaeHylobates lar7070
HylobatidaeSymphalangus syndactylus4220
HominidaeGorilla gorilla7250
HominidaeHomo sapiens5230
HominidaePan paniscus5140
HominidaePan troglodytes7430
HominidaePongo pygmaeus6042

  1. Abbreviations: n, total number of specimens; M, males; F, females; ?, unknown sex.

Additional files

Supplementary file 1

List of extant anthropoid specimens analyzed in this paper.

µCT image stacks were downloaded from MorphoSource digital repository at https://www.MorphoSource.org (Duke University, Durham, NC, USA) or scanned at Paul Sabatier University (PSU, Toulouse, France), the American Museum of Natural History (AMNH; New York, NY, USA) and Centro Nacional de Investigación sobre la Evolución Humana (CENIEH; Burgos, Spain).

https://cdn.elifesciences.org/articles/51261/elife-51261-supp1-v1.xlsx
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