Evolution Of The Ear And Hearing

In 1882, Mayser proposed that the modern ear was derived from the fish lateral line, the acousticolateralis hypothesis, a view that was held for most of a century (Mayser 1882). Mayser described the lateral line as an accessory hearing organ. In 1987, observing embryonic development in salmon, Wilson and Mattocks (Wilson and Mattocks 1887) suggested that the inner ear and lateral line were derived from the same embryonic placode and that the inner ear originated as part of the lateral line. Additional supporting evidence was considered to be the similarity of the hair cells in the lateral line and the inner ear.

In 1974, E. G. Wever wrote an influential paper on the evolution of vertebrate hearing, pointing out that none of the animals thought to be ancestral to vertebrates has an inner ear, so that the inner ear must not be derived from lateral line, but that the lateral line and inner ear share a common ancestor. He believed that bony fishes had the first "real ear." He suggested that the acousticolateralis hypothesis be abandoned in favor of the idea that the inner ear and the lateral line evolved from a common mechanosensory system using hair cells (Wever 1974).

Similarities in the receptor cell structure and the basic function of the ear and auditory system among vertebrate groups, and in the corresponding gene usages, suggest that the ear arose early in the evolution of vertebrates (Popper and Fay 1997). There is a consensus that the earliest inner ear structures were equilibrium receptors rather than auditory receptors. It has been proposed that cochlear ampli fication is ancient (Manley and Koppl 1998) and that the first auditory receptor, the basilar papilla, pinched off from the vestibular organ with the transition of vertebrates from water to land.

Manley and Koppl suggest that this first appeared almost 400 million years ago in lobe-finned fish (Manley and Koppl 1998). However, a basilar papilla seems to have evolved independently several times (Manley and Koppl 1998), after, and perhaps because of, the development of the tympanic ear in the Triassic. This may be one of many examples of the conservation of a basic common ancestral mechanism, like a mechanoreceptor cell or pathway, that has repeatedly been modified for similar purposes. An ability to detect and respond to air or physical vibration apparently evolved many times in invertebrates as well (Michelsen 1992). Animals share common ancestry more closely than was thought in the decades before genetic homologies were identifiable. The distinction between "hearing" and the detection of other forms of environmental vibration is after all a human invention.

Some but not all of these systems involve similar hair cell mechanosensory mechanisms. The near ubiquity of the sensory hair cell in vertebrate ears and the lateral line suggests that it arose early in the evolution of hearing, pressure, or vibration detection. Specialization in form and function, however, suggests that the hair cell has adapted to the specific needs of a variety of vertebrates (Fay and Popper 2000). If precedent (and the results of mouse deafness studies) is a guide, different genetic mechanisms will be found even among animals having very similar physical phenotypes.

Little is known about the evolution of hearing in insects, but it probably evolved from extant mechanoreceptors. Insect auditory receptors are all based on chordo-tonal sensilla—regardless of where the auditory locus is on the body—and the chor-dotonal system is present ontogenetically everywhere. A different part of the chordotonal system has evolved for hearing in different insect lineages (Eberl 1999). Chordotonal organs serve as proprioceptors at the appendicular joints, and at inter-segmental "joints" between the thorax and abdomen and in the abdomen itself.Thus the opportunity for an ear to arise from the chordotonal primordium occurs frequently over the body of a typical insect, given its many joints and appendages.

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