Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods?
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.
Christensen-Dalsgaard
Jakob
J
Center for Sound Communication, Institute of Biology, University of Southern Denmark, DK-5230 Odense M, Denmark. jcd@biology.sdu.dk
Brandt
Christian
C
Wilson
Maria
M
Wahlberg
Magnus
M
Madsen
Peter T
PT
D000818:Animals; D005075:Biological Evolution; D004423:Ear / Q000033:anatomy & histology*; D005399:Fishes / Q000033:anatomy & histology* / Q000235:genetics / Q000502:physiology*; D006309:Hearing / Q000502:physiology*
J Comp Physiol A. 1988 Apr;162(5):633-8
3259629
Nature. 1989 Nov 23;342(6248):425-7
2586610
Electroencephalogr Clin Neurophysiol. 1982 Dec;54(6):629-41
6183096
J Acoust Soc Am. 2010 Aug;128(2):787-94
20707448
Naturwissenschaften. 1990 Mar;77(3):135-7
2342580
Comp Biochem Physiol A Comp Physiol. 1974 Jan;47(1):371-85
4149016
Naturwissenschaften. 1997 Sep;84(9):389-97
9353759
Brain Behav Evol. 1997;50(4):198-212
9310195
J Comp Neurol. 2004 Apr 5;471(3):277-88
14991561
Hear Res. 2011 Mar;273(1-2):25-36
20034550
Brain Res Bull. 2008 Mar 18;75(2-4):365-70
18331899