Divergent otolithic systems in the inner ear of Paranthropus robustus and Australopithecus africanus

Christopher M Smith; Ashley S Hammond; Alessandro Urciuoli; José Braga; Amélie Beaudet; Marine Cazenave; Jeffrey T Laitman; Sergio Almécija

doi:10.1016/j.jhevol.2024.103624

Divergent otolithic systems in the inner ear of Paranthropus robustus and Australopithecus africanus

J Hum Evol. 2024 Dec 14:199:103624. doi: 10.1016/j.jhevol.2024.103624. Online ahead of print.

Authors

Christopher M Smith¹, Ashley S Hammond², Alessandro Urciuoli³, José Braga⁴, Amélie Beaudet⁵, Marine Cazenave⁶, Jeffrey T Laitman⁷, Sergio Almécija⁸

Affiliations

¹ Division of Anthropology, American Museum of Natural History, New York, NY, USA; New York Consortium in Evolutionary Primatology, New York, NY, USA. Electronic address: csmith2@amnh.org.
² Division of Anthropology, American Museum of Natural History, New York, NY, USA; New York Consortium in Evolutionary Primatology, New York, NY, USA.
³ Universitat Autònoma de Barcelona, Barcelona, Spain; Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain; Division of Paleoanthropology, Senckenberg Research Institute and Natural History Museum, Frankfurt, Germany; Universidad de Alcalá, Cátedra de Otoacústica Evolutiva y Paleoantropología (HM Hospitales-UAH), Departamento de Ciencias de la Vida, Alcalá de Henares 28871, Madrid, Spain.
⁴ Centre for Anthropobiology and Genomics of Toulouse, Université de Toulouse, Toulouse, France; Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa.
⁵ Laboratoire de Paléontologie, Évolution, Paléoécosystèmes et Paléoprimatologie (PALEVOPRIM), UMR 7262 CNRS & Université de Poitiers, 6 Rue Michel Brunet, 86000 Poitiers, France; Department of Archaeology, University of Cambridge, Cambridge, United Kingdom; School of Geography, Archaeology and Environmental Studies, University of the Witwatersrand, Johannesburg, South Africa.
⁶ Department of Human Origins, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany; Department of Anatomy, University of Pretoria, Pretoria, South Africa; Division of Anthropology, American Museum of Natural History, New York, NY, USA.
⁷ Center for Anatomy and Functional Morphology, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁸ Division of Anthropology, American Museum of Natural History, New York, NY, USA; Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain; New York Consortium in Evolutionary Primatology, New York, NY, USA.

PMID: 39675267
DOI: 10.1016/j.jhevol.2024.103624

Abstract

The bony labyrinth of the inner ear houses the sensory end-organs responsible for balance (otolithic system in the utricle and saccule, and semicircular canal system) and hearing (cochlea). Study of the bony labyrinth has revealed considerable morphological diversity in the hominin lineage (semicircular canals and cochleae) and aided in reconstructing essential aspects of primate evolution, including positional behavior, audition, and phylogenic affinities. However, evidence of evolutionary change in the hominin otolithic system remains elusive. Such morphological variation in these gravitoinertial sensory end-organs may suggest functional differences as their geometry is linked with positional behavior. We approach the question of evolutionary morphological change in the hominin otolithic system by examining bony vestibule morphology in two South African hominin taxa Paranthropus robustus (n = 9) and Australopithecus africanus (n = 6), compared to extant hominids (Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). We use landmark-based shape analyses of 78 extant hominid inner ears by means of virtual three-dimensional models derived from micro-computed tomography scans. Thirty bony landmarks were chosen to approximate otolithic organ morphology and relative configuration. Results show a distinctive morphology in P. robustus compared to A. africanus and extant hominids. Specifically, P. robustus exhibits anterolateral-posteromedial compression in bony otolithic organ structure, reducing the size of the saccule and vestibular aqueduct. In contrast, A. africanus exhibits a modern-human-like otolithic system. This newfound morphological diversity identifies unique bony features of the P. robustus inner ear which: 1) offers potential evidence for differential positional behavior between P. robustus and A. africanus and 2) presents osteological markers to be used in taxonomic identification of P. robustus remains and in future assessments of Paranthropus classification.

Keywords: Geometric morphometrics; Hominin; Inner ear; Vestibular system.