Hearing evolution across the air-water interface: lessons from comparative audiometry in turtles and salamanders

Abstract

The physical differences between water and air present unique challenges to organisms living in both environments, including challenges to the sense organs. In the auditory system, acoustic impedance mismatch is a challenge to airborne sound detection, but not aquatic sound detection. Evolutionary transitions of vertebrates across aquatic and terrestrial environments are often associated with changes in sensory systems. Comparative studies of hearing in amphibious taxa that have diversified across aquatic and terrestrial environments could illuminate the payoffs and constraints affecting hearing in aquatic-terrestrial transitions. Using evoked potentials, I collected aquatic and aerial auditory sensitivities from two amphibious tetrapod orders, Testudines and Caudata, to test the hypothesis that terrestrial clades have evolved heightened aerial sensitivity relative to aquatic ancestors. I also tested whether two aspects of extra-tympanic hearing in salamanders confer advantages to aerial auditory sensitivity: (1) metamorphosis and (2) body wall vibrations over the lungs. In Testudines, I found a positive association between terrestrial specialization and aerial sensitivity, although the fossorial Gopherus polyphemus showed reduced high frequency sensitivity. A broader survey of audiograms in the literature supports this positive association. Aquatic sensitivity of terrestrial Terrapene carolina was comparable to that of aquatic species, indicating that augmented aerial sensitivity is not necessarily associated with marked aquatic hearing loss. In Caudata, I failed to find a comparable positive association: aerial sensitivity of the terrestrial Plethodon glutinosus did not exceed that of the more sensitive aquatic species, and metamorphosis did not increase aerial sensitivity in Ambystoma talpoidem or Notophthalmus viridescens. The relationship between aerial and aquatic sensitivity varied at different frequencies and for different species. In particular, relative to the smaller species tested, the large aquatic Amphiuma means exhibited better aquatic-aerial carryover of auditory sensitivity at low frequencies and poorer carryover at high frequencies. Experimental blocking of the body wall over the lungs via submersion under a water surface did not change auditory thresholds in A. talpoideum or N. viridescens, failing to support a lung-based aerial auditory pathway. This dissertation develops our understanding of vertebrate hearing across aquatic-terrestrial transitions.