Biology Letters
Restricted accessNeurobiology

Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?

Published:https://doi.org/10.1098/rsbl.2010.0636

    Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.

    References

    • 1
      Clack J. A.. 1989Discovery of the earliest-known tetrapod stapes. Nature 342, 425–427.doi:10.1038/342425a0 (doi:10.1038/342425a0). Crossref, PubMed, ISIGoogle Scholar
    • 2
      Clack J. A.. 1997The evolution of tetrapod ears and the fossil record. Brain, Behav. Evol. 50, 198–212.doi:10.1159/000113334 (doi:10.1159/000113334). Crossref, PubMed, ISIGoogle Scholar
    • 3
      Christensen-Dalsgaard J.& Carr C. E.. 2008Evolution of a sensory novelty: tympanic ears and the associated neural processing. Brain Res. Bull. 75, 365–370.doi:10.1016/j.brainresbull.2007.10.044 (doi:10.1016/j.brainresbull.2007.10.044). Crossref, PubMed, ISIGoogle Scholar
    • 4
      Kalmijn J.. 1989Functional evolution of lateral line and inner ear sensory systems. The mechano sensory lateral line (eds , Coombs S., Görner P.& Münz H.), pp. 187–215. New York, NY: Springer. Google Scholar
    • 5
      Popper A. N.& Fay R. R.. In press. Rethinking sound detection by fishes. Hear. Res. (doi:10.1016/j.heares.2009.12.023). ISIGoogle Scholar
    • 6
      Popper A. N., Fay R. R., Platt C.& Sand O.. 2003Sound detection mechanisms and capabilities of teleost fishes. Sensory processing in aquatic environments (eds , Collin S. P.& Marshall N. J.), pp. 3–38. New York, NY: Springer. CrossrefGoogle Scholar
    • 7
      Platt C., Jørgensen J. M.& Popper A.. 2004The inner ear of the lungfish Protopterus. J. Comp. Neurol. 3, 277–288. Crossref, ISIGoogle Scholar
    • 8
      Zardoya R.& Meyer A.. 1997Molecular phylogenetic information on the identity of the closest living relative(s) of land vertebrates. Naturwissenschaften 84, 389–397.doi:10.1007/s001140050415 (doi:10.1007/s001140050415). Crossref, PubMed, ISIGoogle Scholar
    • 9
      Corwin J. T., Bullock T. H.& Schweitzer J.. 1982The auditory brain stem response in five vertebrate classes. Electroencephalogr. Clin. Neurophysiol. 54, 629–641.doi:10.1016/0013-4694(82)90117-1 (doi:10.1016/0013-4694(82)90117-1). Crossref, PubMedGoogle Scholar
    • 10
      Brandt C., Andersen T.& Christensen-Dalsgaard J.. 2008 In Auditory signal processing in hearing-impaired listeners. Int. Symp. on Auditory and Audiological Research (eds , Dau T., Buchholz J. M., Harte J. M.& Christiansen T. U.), pp. 241–274. Copenhagen, Denmark: Centertryk. Google Scholar
    • 11
      Christensen-Dalsgaard J., Breithaupt T.& Elepfandt A.. 1990Underwater hearing in the clawed frog Xenopus laevis. Tympanic motion studied with laser vibrometry. Naturwissenschaften 77, 135–137.doi:10.1007/BF01134478 (doi:10.1007/BF01134478). Crossref, PubMed, ISIGoogle Scholar
    • 12
      Chapman C. J.& Sand O.. 1974Field studies of hearing in two species of flatfish, Pleuronectes platessa and Limanda limanda. Comp. Biochem. Physiol. 47, 371–385. CrossrefGoogle Scholar
    • 13
      Brittan-Powell E. F., Christensen-Dalsgaard J., Tang Y., Carr C.& Dooling R. J.. 2010The auditory brainstem response in two lizard species. J. Acoust. Soc. Am. 128, 787–794.doi:10.1121/1.3458813 (doi:10.1121/1.3458813). Crossref, PubMed, ISIGoogle Scholar
    • 14
      Christensen-Dalsgaard J.& Jørgensen M. B.. 1988The response characteristics of vibration-sensitive saccular fibers in the grassfrog, Rana temporaria. J. Comp. Physiol. A 162, 633–638.doi:10.1007/BF01342638 (doi:10.1007/BF01342638). Crossref, PubMed, ISIGoogle Scholar
    • 15
      Clack J. A.& Allin E.. 2004The evolution of single- and multiple-ossicle ears in fishes and tetrapods. Evolution of the vertebrate auditory system (eds , Manley G. A., Popper A. N.& Fay R. R.), pp. 128–163. New York, NY: Springer. Google Scholar
    • 16
      Fritzsch B.. 1999Hearing in two worlds. Theoretical and actual adaptive changes of the aquatic and terrestrial ear. Comparative hearing: fish and amphibians (eds , Fay R. R.& Popper A. N.), pp. 15–42. New York, NY: Springer. Google Scholar
    • 17
      Lombard R. E.& Bolt J.. 1979Evolution of the tetrapod ear: an analysis and reinterpretation. Biol. J. Linn. Soc. 11, 19–76.doi:10.1111/j.1095-8312.1979.tb00027.x (doi:10.1111/j.1095-8312.1979.tb00027.x). Crossref, ISIGoogle Scholar