Evolutionary modularity of the primate vestibular system: Morphological distinction of otolithic and canalicular organs.

Abstract

The mammalian inner ear is traditionally divided into two systems: the peripheral vestibular system (for balance) and the cochlea (for hearing). This bipartite model has shaped our understanding of inner ear evolution, function, and pathology. However, it groups the semicircular ducts (which detect angular velocity) and otolithic organs (which detect linear acceleration, vibration, and head tilt) into a single peripheral vestibular system, overlooking key differences in their structure and function. Using advances in imaging technology, we investigate whether the otolithic system is evolutionarily and structurally distinct from the semicircular ducts, with a focus on primates. Specifically, we assess modularity and phylogenetic signal in the inner ear across 14 primate species using landmark-based 3D geometric morphometrics within a phylogenetic framework. Our results reveal previously unrecognized modularity in the primate peripheral vestibular system. The semicircular canals and otolithic organs show stronger integration within their own structures rather than with each other. Furthermore, these two systems show divergent evolutionary trajectories in both size and shape, particularly among hominoids. These findings challenge the traditional bipartite model of the inner ear. Instead, a tripartite framework comprising distinct cochlear, canalicular, and otolithic systems better reflects the structural, functional, and evolutionary complexity of the primate inner ear. This revised model reshapes perspectives on vestibular system organization and has implications for studies on balance, sensory adaptation, and inner ear disorders.