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Why Comparative Hearing and Evolution
For well over 100 years, investigators have pondered questions regarding the evolutionary origin of the vertebrate
ear and about how the ear evolved from its most primitive form to that found in modern mammals. The earliest ideas for
the origin of the ear, called the acousticolateralis hypothesis, suggested that the ear evolved from the lateral line
(reviewed in Popper et al., 1992). A variety of studies suggested a series of evolutionary changes from the primitive
ear to that of modern mammals (see van Bergeijk, 1967). More recent investigators, and particularly those using modern
anatomical and physiological methods, now suggest that while the ear and lateral line may share a common ancestor,
these are two distinct systems that are unrelated in terms of one giving rise to the other
(see Popper et al., 1992). Moreover, as pointed out by Wever (e.g., 1974), we must now question whether there was a
steady sequence in the evolution of the vertebrate ear, or whether, in fact, the ear, and regions of the ear,
evolved multiple times in the course of vertebrate history, much as very similar ears evolved multiple times in the
evolution of invertebrates (e.g., Budelmann, 1992; Hoy, 1992; Popper and Fay, 1997; Fay and Popper, 2000).
The diversity of ear structure and of auditory systems among vertebrates is extraordinarily large, and very few data are
available even now that help us answer questions relating to the evolution of the auditory system. At the same time,
it is likely that we may learn more about evolution of sensory systems from studying the auditory system than from any
other sensory system. The reason for this is simple. There is a potential wealth of information about evolutionary changes
in the ear lying in the fossil record - something that is not available for any other vertebrate sensory system
(e.g., Clack, 1997). Moreover, the striking comparative material available for each of the different levels of the
vertebrate auditory system (from periphery to CNS) is far richer than for any other sensory system. In essence, the very
fact that the ear may have evolved multiple times (see Fritzsch, 1992, p. 790) provides a rich body of comparative data upon
which to evaluate evolution of the ear.
The comparative provides a basis for asking questions that cannot be as readily dealt with using more traditional animal
models (see Hodos, 1997). The comparative approach may reveal remarkable similarity of design; these may result from the
constraints of signal analysis or from homology. On the other hand, differences between systems are equally as instructive,
in that they may reflect the action of evolution upon different substrates, and the different requirements of each system.
Clearly, recent understanding of the study of post-embryonic hair cell development and regeneration has benefited greatly
from the comparative approach that included studies of elasmobranchs (Corwin, 1981), fish (Popper and Hoxter, 1984),
amphibians (Corwin, 1985) and birds (e.g., Corwin and Cotanche, 1988; Ryals and Rubel, 1988). Similarly, our knowledge of
the function of sensory hair cells is based upon studies of species as diverse as fishes (e.g., Flock, 1977),
frogs (e.g., Gillespie and Hudspeth, 1991) and turtles (e.g., Crawford and Fettiplace, 1981).
References
Budelmann, B.-U. (1992) Hearing of nonarthropod invertebrates. In: Webster, D.B., Fay, R.R. and Popper, A.N. eds. Comparative Evolutionary Biology of Hearing, Springer Verlag, NY., pp. 141-155.
Clack, J.A. (1997) The evolution of tetrapod ears and the fossil record. Brain Behav Evol, 50:213-221.
Corwin, J. T. (1981). Postembryonic production and aging in inner ear hair cells in sharks. J. Comp. Neurol., 201, 541 553.
Corwin, J. T. (1985). Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc. Natl. Acad. Sci. USA, 82, 3911 3915.
Corwin, J.T., and D.A. Cotanche (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772-1774.
Costello, L. C., Franklin, R. B., and Ashe, W. K. (1994). Black physiologists B Where are they? The Physiologist 37:284-286.
Crawford, A. C. and Fettiplace, R. (1981). An electrical tuning mechanism in turtle cochlear hair cells. J. Physiol. 312:377-412.
Fay, R. R. and Popper, A. N. (2000). Evolution of hearing in vertebrates: The inner ears and processing. Hear. Res., 149:1-10.
Fields, C. D. (1998). Trouble along the science pipeline. Black Issues in Higher Education, March 19, 1998, pp. 14-15.
Flock, Å.(1977). Physiological properties of sensory hairs in the ear. In Psychophysics and Physiology of Hearing. Evans, E.F. & Wilson, J.P. (eds.). London: Academic Press.
Fritzsch, B. (1992) The water-to-land transition: Evolution of the tetrapod basilar papilla, middle ear, and auditory nuclei. In: Webster, D.B., Fay, R.R. and Popper, A.N. eds. Comparative and Evolutionary Biology of Hearing, Springer Verlag, NY., pp. 351-376.
Gillespie, P.G. and Hudspeth, A. J. (1991). High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J. Cell Biol. 112: 625-640.
Hodos, W. (1997) Evolution of sensory pathways in vertebrates. Brain, Behav, Evol, 50:189-198.
Hoy, R. R. (1992) The evolution of hearing in insects as an adaptation to predation from bats. In: Webster, D.B., Fay, R.R. and Popper, A.N. eds. Comparative and Evolutionary Biology of Hearing, Springer Verlag, NY., pp. 115-130.
Massey, W. (1992). A success story amid decades of disappointment. Science 258:1177-1180.
Popper, A.N. and Hoxter, B. (1984). Growth of a fish ear: I. Quantitative analysis of sensory hair cell and ganglion cell proliferation. Hearing Res., 15:133 142.
Popper, A.N. and Fay, R.R. (1997) Evolution of the ear and hearing: Issues and questions. Brain, Behav, Evol, 50:213-221.
Popper, A.N., Platt, C. and Edds, P. (1992). Evolution of the Vertebrate Inner Ear: An Overview of Ideas. In: Webster, D.B., Fay, R.R. and Popper, A.N. eds. Comparative Evolutionary Biology of Hearing, Springer Verlag, NY., pp. 49-57.
Ryals, B.M, and E.W. Rubel (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774-1776.
van Bergeijk, W. A. (1967). Introductory comments on lateral line function. In Lateral Line Detectors. P. Cahn, ed. pp. 73 81. Indiana Univ. Press. Bloomington, Indiana.
Webster, D.B., Fay, R.R. and Popper, A.N. eds. (1992). Evolutionary Biology of Hearing, Springer Verlag, New York.
Wever, E. G. (1974). The evolution of vertebrate hearing. Pages 423 454 in W. D. Keidel and W. D. Neff, eds. Handbook of Sensory Physiology, Vol. V/1, Auditory System. Springer Verlag, Berlin.
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