Lungfish Hearing: Implications for the evolution of the tetrapod middle ear

Recent research has shown that tympanic middle ears
evolved independently in the major vertebrate groups and
represent independent experiments in terrestrial hearing.
Furthermore, the tympanic ear emerged quite late – ap
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proximately 120 mya after the origin of the tetrapods and
approximately 70 my after the first truly terrestrial tetrapods
emerged. One of the major challenges is to understand the
transitional stages from tetrapod ancestors to the tympanic
tetrapod ear, for example how a non-tympanic ear functions
in terrestrial hearing. Lungfish are the closest living relatives
of the tetrapods, and the ear of lungfish may be similar to the
ear of theearly tetrapods.
We have studied the sensitivity of African lungfish to air-borne
sound, underwater sound and vibrations. We show that lung
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fish detect underwater sound pressure via pressure-to-par
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ticle motion transduction by air volumes in their lungs and
that lungfish detect air-borne sound by sound-induced head
vibrations, resulting in a limited sensitivity to low-frequen
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cy sound (lowest thresholds from 80 dB SPL). Adiditionally,
lungfish are sensitive to substrate vibration with a sensitivity
comparable to anurans and urodeles.
Based on ABR and vibration measurements also on amphib
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ians, lizards, snakes and alligators we can outline scenarios
for the initial adaptations of the middle ear to non-tympanic
hearing and assess the selection pressures later adapting the
middle ear for tympanic hearing. Hearing by bone conduc
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tion, sound induced vibrations of the skull, is found in snakes
and some earless frogs, whereas urodeles and other earless
frogs are more sensitive than predicted from sound-induced
skull vibrations and may have specialized pathways to the
inner ear. We propose four stages : 1) the unspecialized cros
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sopterygian ear with immobile middle ear bone, 2) increased
inner ear frequency ranges, 3) mobile middle ear structures
and 4) the tympanic middle ear.