The evolution of the vestibular apparatus in apes and humans

Abstract

Phylogenetic relationships among extinct hominoids (apes and humans) are controversial due to pervasive homoplasy and the incompleteness of the fossil record. The bony labyrinth might contribute to this debate, as it displays strong phylogenetic signal among other mammals. However, the potential of the vestibular apparatus for phylogenetic reconstruction among fossil apes remains understudied. Here we test and quantify the phylogenetic signal embedded in the vestibular morphology of extant anthropoids (monkeys, apes and humans) and two extinct apes (Oreopithecus and Australopithecus) as captured by a deformation-based 3D geometric morphometric analysis. We also reconstruct the ancestral morphology of various hominoid clades based on phylogenetically-informed maximum likelihood methods. Besides revealing strong phylogenetic signal in the vestibule and enabling the proposal of potential synapomorphies for various hominoid clades, our results confirm the relevance of vestibular morphology for addressing the controversial phylogenetic relationships of fossil apes.

Variation of bony labyrinthine morphology in Mio−Plio−Pleistocene and modern anthropoids

“…Overall, these studies demonstrate that the morphology of the bonylabyrinth is an ideal source of information for addressing questions about thelocomotion, phylogenetic relationships and taxonomy of extant and fossil primates. One question of fundamental interest is how the bony labyrinthine morphology changed over the course of anthropoid evolution (see also Urciuoli et al, 2020). Here we emplace key fossil hominoid primates from the Mio–Plio–Pleistocene within the extant species morphospace in order to clarify the evolutionary patterns that characterize the hominid (great ape and human) clade in more detail than currently known (Spoor et al, 2007).…”

Reassessment of the phylogenetic relationships of the late Miocene apes Hispanopithecus and Rudapithecus based on vestibular morphology

“…Differences in volumetric proportions of the SCs have been related to locomotor adaptations, because they directly affect the sensitivity and steadiness of the SCs in response to angular accelerations (5,56). Hence, the moderately stout SCs of the LCA of crown hominids indicate that it showed a slow type of locomotion, which was present, to a large extent, also in the LCA of crown hominoids, as previously inferred based on the size of the SC radius alone (41).…”

“…Allometric regressions of SC volume vs. length were performed separately for hominoids and the rest of anthropoids included in the sample (Fig. 2a; measurements for the dryopiths are given in Supplementary Table 1) because it has been previously shown that the former display an allometric grade shift toward relatively higher volumes at a comparable length once size-scaling effects have been taken into account (5), with only minimal overlap. Hispanopithecus falls above the hominid regression line, while Rudapithecus is situated more (RUD 77) or less (RUD 200) below the line, close to Nacholapithecus, but in all cases within the range of extant hominids and well above the regression line of other anthropoids (Fig.…”

“…These similarities particularly concern the volumetric proportions of the SCs as well as the size of the latter relative to the vestibular recesses. Volumetric proportions, as reflected by the ratio between the volume and the length of the SCs, appear particularly relevant given that an allometric grade shift has been previously identified to characterize all extant hominids, so that they display relatively more voluminous SCs than other anthropoids (including hylobatids) at comparable lengths (5). The derived condition of hominids has been linked with locomotion (5), but is noteworthy that chimpanzees, bonobos, and gorillas are slightly more variable in SC volumetric proportions than orangutans and humans.…”

“…The morphology of the semicircular canals (SCs), which partly constitute the inner ear's bony labyrinth, has been classically related to locomotion (36)(37)(38)(39)(40)(41)(42). However, several studies have highlighted the possibility of inferring phylogenetic relatedness based on this portion of the inner ear morphology (43)(44)(45)(46)(47) Recently, it has been shown that this anatomical structure also embeds a strong phylogenetic signal among catarrhine primates by means of 3D geometric morphometric (3DGM) analyses (5,(47)(48)(49), thus being potentially useful to test phylogenetic hypotheses for extinct hominoids. Previous studies relied on the SC radius of Rudapithecus hungaricus and Hispanopithecus laietanus to infer slow and deliberate arboreal locomotion for these species (41).…”