Hearing without a tympanic ear

Abstract

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.

Central projections of auditory nerve fibers in the western rat snake (Pantherophis obsoletus)

“…Therefore, it is reasonable to conclude that snakes, at least to some extent, detect vibrations using the auditory endorgan, the basilar papilla, and centrally process vibrational stimuli in the ascending auditory pathways. While seismic or aquatic vibration are primarily detected by otolithic endorgans such as the saccule in fish and amphibians (Christensen‐Dalsgaard & Buhl Jørgensen, 1988; Christensen‐Dalsgaard & Carr, 2008; Popper & Fay, 1999), nonotolithic endorgans such as the organ of Corti in mammals and the amphibian papilla in amphibians also facilitate vibration sensing (Capshaw et al., 2022; Christensen‐Dalsgaard & Narins, 1993; Stenfelt, 2013; Yu et al., 1991). In snakes, it has been hypothesized that vibrational stimuli impinging on the lower jaw or quadrate may cause movement of the stapes relative to the oval window, causing fluid displacement in the inner ear and stimulation of the basilar papilla (Friedel et al., 2008; Wever, 1978).…”

The anatomical basis of amphibious hearing in the American alligator (Alligator mississippiensis)

“…The specialized cephalic receptor for pressure waves, the tympanic membrane or eardrum, has evolved multiple times in vertebrates (e.g., Capshaw et al, 2022). Many of the evolutionary radiations of vertebrates with tympanic hearing include amphibious taxa (e.g., Clack, 2002).…”

Rich acoustic landscapes dominated the Mesozoic

“…Out of water, the impedance mismatch between air and animal tissue requires specialized sound detection organs, and multiple insect clades have independently come up with the same solution to this challenge: tympanic ears. In fact, land vertebrates have also converged on similar tympanic morphologies ( 8 ). Tympanal organs in insects have three primary components: a tympanal membrane (i.e., eardrum), an air-filled cavity behind the tympanum, and a chordotonal sensory organ that encodes the received sound into neuronal firings.…”

“…Prior to the evolution of airborne acoustic songs, most biologically relevant sound was clustered in the low frequencies, as it is today ( 16 ). Phylogenetic reconstructions indicate that the vertebrate tympanic ear evolved multiple times in the early Triassic, allowing for better hearing than atympanic ears, particularly at higher frequencies ( 8 ). These tympanic organs are precisely the types of ears that would allow land vertebrates to successfully eavesdrop on katydid song.…”