The tympanic middle ear is an adaptive sensory novelty that evolved multiple times in all of the major terrestrial tetrapod groups to overcome the impedance mismatch generated when aerial sound encounters the air-skin boundary. Many extant tetrapod species have lost their tympanic middle ears, yet they retain the ability to detect airborne sound. In the absence of a functional tympanic ear, extratympanic hearing may occur via the resonant qualities of air-filled body cavities, sensitivity to seismic vibration, and/or bone conduction pathways to transmit sound from the environment to the ear. We used auditory brainstem response recording and laser vibrometry to assess the contributions of these extratympanic pathways for airborne sound in atympanic salamanders. We measured auditory sensitivity thresholds in eight species and observed sensitivity to low frequency sound and vibration from 0.05-1.2 kHz and 0.02-1.2 kHz, respectively. We determined that sensitivity to airborne sound is not facilitated by the vibrational responsiveness of the lungs or mouth cavity. We further observed that, although seismic sensitivity likely contributes to sound detection under naturalistic scenarios, airborne sound stimuli presented under experimental conditions did not produce vibrations detectable to the salamander ear. Instead, threshold-level sound pressure is sufficient to generate translational movements in the salamander head, and these sound-induced head vibrations are detectable by the acoustic sensors of the inner ear. This extratympanic hearing mechanism mediates low frequency sensitivity in vertebrate ears that are unspecialized for the detection of aerial sound pressure, and may represent a common mechanism for terrestrial hearing across atympanic tetrapods.

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Lungless salamanders (Family Plethodontidae) form a highly speciose group that has undergone spectacular adaptive radiation to colonize a multitude of habitats. Substantial morphological variation in the otic region coupled with great ecological diversity within this clade make plethodontids an excellent model for exploring the ecomorphology of the amphibian ear. We examined the influence of habitat, development, and vision on inner ear morphology in 52 plethodontid species. We collected traditional and 3D geometric morphometric measurements to characterize variation in size and shape of the otic endocast and peripheral structures of the salamander ear. Phylogenetic comparative analyses demonstrate structural convergence in the inner ear across ecologically similar species. Species that dwell in spatially complex microhabitats exhibit robust, highly curved semicircular canals suggesting enhanced vestibular sense, whereas species with reduced visual systems demonstrate reduced canal curvature indicative of relaxed selection on the vestibulo‐ocular reflex. Cave specialists show parallel enlargement of auditory‐associated structures. The morphological correlates of ecology among diverse species reveal underlying evidence of habitat specialization in the inner ear and suggest that there exists physiological variation in the function of the salamander ear even in the apparent absence of selective pressures on the auditory system to support acoustic behavior.

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The ability to sense and localize sound is so advantageous for survival that it is difficult to understand the almost 100 million year gap separating the appearance of early tetrapods and the emergence of an impedance-matching tympanic middle ear – which we normally regard as a prerequisite for sensitive hearing on land – in their descendants. Recent studies of hearing in extant atympanate vertebrates have provided significant insights into the ancestral state(s) and the early evolution of the terrestrial tetrapod auditory system. These reveal a mechanism for sound pressure detection and directional hearing in ‘earless’ atympanate vertebrates that may be generalizable to all tetrapods, including the earliest terrestrial species. Here, we review the structure and function of vertebrate tympanic middle ears and highlight the multiple acquisition and loss events that characterize the complex evolutionary history of this important sensory structure. We describe extratympanic pathways for sound transmission to the inner ear and synthesize findings from recent studies to propose a general mechanism for hearing in ‘earless’ atympanate vertebrates. Finally, we integrate these studies with research on tympanate species that may also rely on extratympanic mechanisms for acoustic reception of infrasound (<20 Hz) and with studies on human bone conduction mechanisms of hearing.

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