Evolution of a sensory novelty: Tympanic ears and the associated neural processing

Journal of Experimental Biology

Brandt

et al. 2012

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SUMMARYSnakes lack both an outer ear and a tympanic middle ear, which in most tetrapods provide impedance matching between the air and inner ear fluids and hence improve pressure hearing in air. Snakes would therefore be expected to have very poor pressure hearing and generally be insensitive to airborne sound, whereas the connection of the middle ear bone to the jaw bones in snakes should confer acute sensitivity to substrate vibrations. Some studies have nevertheless claimed that snakes are quite sensitive to both vibration and sound pressure. Here we test the two hypotheses that: (1) snakes are sensitive to sound pressure and (2) snakes are sensitive to vibrations, but cannot hear the sound pressure per se. Vibration and sound-pressure sensitivities were quantified by measuring brainstem evoked potentials in 11 royal pythons, Python regius. Vibrograms and audiograms showed greatest sensitivity at low frequencies of 80-160Hz, with sensitivities of -54dBre.1ms -2 and 78dBre.20mPa, respectively. To investigate whether pythons detect sound pressure or sound-induced head vibrations, we measured the sound-induced head vibrations in three dimensions when snakes were exposed to sound pressure at threshold levels. In general, head vibrations induced by threshold-level sound pressure were equal to or greater than those induced by threshold-level vibrations, and therefore sound-pressure sensitivity can be explained by sound-induced head vibration. From this we conclude that pythons, and possibly all snakes, lost effective pressure hearing with the complete reduction of a functional outer and middle ear, but have an acute vibration sensitivity that may be used for communication and detection of predators and prey.Supplementary material available online at

Section: Pamentioning

confidence: 99%

Hearing with an atympanic ear: good vibration and poor sound-pressure detection in the royal python,Python regius

Christensen

Journal of Experimental Biology

Brandt

et al. 2012

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“…. The stimulus presentation, ABR acquisition, equipment control and data management are similar to those in prior studies [2,22]. Stimulation, recording and data analysis were performed by custom software (QuickABR) running on a PC and a digital signal processor (Tucker-Davis Technologies (TDT; Gainesville, FL, USA) RM2).…”

Section: Methodsmentioning

confidence: 99%

Specialization for underwater hearing by the tympanic middle ear of the turtle,Trachemys scripta elegans

Brandt

Willis

et al. 2012

Proc. R. Soc. B.

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Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500-600 Hz with a maximum of 300 mm s 21 Pa 21 , approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300-500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20-30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.

“…This problem may not have been solved until the convergent evolution of tympanic middle ears in all the tetrapod lineages during the early Triassic (Christensen-Dalsgaard and Carr, 2008;Clack, 1997;Clack, 2011). Consequently, there may have been a period of up to 100 million years when early tetrapods were unable to hear aerial sound.…”

Section: Introductionmentioning

confidence: 99%

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Christensen

Journal of Experimental Biology

Madsen

2015

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In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-toparticle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods.