Manley, G. A. (1986). The evolution of the mechanisms of frequency selectivity in vertebrates. In: Auditory Frequency Selectivity (Moore, B.C.J., Patterson, R.D., eds.), Plenum, New York, 63-72

Modern vertebrates display an almost bewildering variety of inner-ear structure and function. Any attempt to understand this variety must begin with a search for unifying principles. Evolution is, without question, the most important unifying principle in the biological sciences... All vertebrate hair-cell systems are frequency selective, presumably due to early selection pressures for distinguishing different signals by means of their spectral content. In addition, all systems are tonotopically organized...

FREQUENCY SELECTIVITY DUE TO ELECTRICAL PROPERTIES OF THE CELL The cell membranes of tuberous receptors of weakly-electric fish (Hopkins, 1976) and of many fish neuromast cells (Suga, 1967) respond in a frequency-selective fashion to electrical changes outside the body... Recent extensive studies of a turtle papilla have demonstrated a tonotopic organization along its length, with frequencies varying from about 70 up to 670 Hz... Similarities to the behaviour of electroreceptors are seen in the fact that in many nonmammals, the frequency selectivity of tuning is also temperature sensitive ... Thus, in many nonmammalian inner ears, there is strong evidence for an involvement of electrical tuning in the frequency selectivity of hair cells...

FREQUENCY SELECTIVITY DUE TO THE MECHANICAL PROPERTIES OF HAIR CELLS AND THEIR ACCESSORY STRUCTURES The situation with regard to mechanical tuning is very much more complicated than with electrical tuning. This is because a variety of accessory structures can be involved in mechanical filtering -- not only the hair cells themselves...

MAMMALS No evidence exists in mammals for electrical tuning of the kind described above - the tuning of single fibres is not temperature sensitive, there are no preferred intervals in the spontaneous activity and there are no reports of "ringing" in hair-cell recordings (Russell et al., 1986)...

THE QUESTION OF SPACE ...The frequency range of sensitivity is rather constant in all lizards (up to 4-5 kHz CF), so that in longer basilar papillae, more space is devoted to each octave. If we take the temperature effect into account (a shift of 0.06 octaves/oC), the upper limit of hearing in most birds (6-7 kHz CF) is the same as in reptiles. The very much higher upper limits in mammals may in part depend on the changed middle-ear structure, but it cannot be excluded that the interactive selectivity mechanism in the mammalian organ of Corti functions more efficiently at these higher frequencies than the mechanisms operative in nonmammals. When we compare the space available for encoding an octave in mammals(e.g., 2.5 mm in the guinea pig) with that in nonmammals (Fig.1), it is obvious that mammals in general not only possess a longer cochlea, but that they also devote a lot more space (and therefore hair cells) to each octave. In some cases, more space is devoted to a frequency region of particular importance (e.g., in some bats).

Thus, while the mammals may have abandoned the use of their hair-cell ion channels for the production of strong electrical tuning, they have evolved a more elaborate and specialized system of tuning, with the inner hair cells being detectors of fluid motions resulting from the complex mechanical interaction of outer hair cells and their associated accessory structures. It is possible that this mechanism arose originally for higher-frequency analysis dur to inherent frequency limitations of the more primitive mechanisms...