Most vertebrates have evolved a tympanic middle ear that enables effective hearing of airborne sound on land. Although inner ears develop during the tadpole stages of toads, tympanic middle ear structures are not complete until months after metamorphosis, potentially limiting the sensitivity of post-metamorphic juveniles to sounds in their environment. We tested the hearing of five species of toads to determine how delayed ear development impairs airborne auditory sensitivity. We performed auditory brainstem recordings to test the hearing of the toads and used micro-computed tomography and histology to relate the development of ear structures to hearing ability. We found a large (14–27 dB) increase in hearing sensitivity from 900 to 2500 Hz over the course of ear development. Thickening of the tympanic annulus cartilage and full ossification of the middle ear bone are associated with increased hearing ability in the final stages of ear maturation. Thus, juvenile toads are at a hearing disadvantage, at least in the high-frequency range, throughout much of their development, because late-forming ear elements are critical to middle ear function at these frequencies. We discuss the potential fitness consequences of late hearing development, although research directly addressing selective pressures on hearing sensitivity across ontogeny is lacking. Given that most vertebrate sensory systems function very early in life, toad tympanic hearing may be a sensory development anomaly.
The authors declare no competing or financial interests.
M.C.W. and K.L.H contributed to all aspects of the project including experimental design, data collection, data analysis, and drafting and revising the article. J.C.-D. contributed to experimental design, data collection, drafting and revising the article.
Funding for this study was provided by the Danish National Science Foundation (DFF1323-00132), the US National Science Foundation (NSF #IOS-13503461350346 and OISE-1157779) as well as a Grants-In-Aid-of-Research fellowship from Sigma Xi (G20111015158047).
- Received May 18, 2016.
- Accepted August 5, 2016.
- © 2016. Published by The Company of Biologists Ltd