The form and function of the ears of modern land vertebrates cannot be understood without knowing how they evolved.

Unlike eyes, which are generally instantly recognizable, ears differ greatly in their appearance throughout the animal kingdom. Some hearing structures may not be visible at all. For example, camouflaged in the barn owl’s facial ruff—a rim of short, brown feathers surrounding the bird’s white face—are clusters of stiff feathers that act as external ears on either side of its head. These feather structures funnel sound collected by two concave facial disks to the ear canal openings, increasing the bird’s hearing sensitivity by 20 decibels—approximately the difference between normal conversation and shouting. Similar increases in sensitivity result from the large and often mobile external structures, or pinnae, of many mammals, such as cats and bats. Internally, the differences among hearing organs are even more dramatic.

Although fish can hear, only amphibians and true land vertebrates—including the aquatic species that descended from them, such as whales and pinnipeds—have dedicated hearing organs. In land vertebrates belonging to the group Amniota, including lizards, birds, and mammals, sound usually enters through an external canal and impinges on an eardrum that is connected through middle-ear bones to the inner ear. There, hundreds or thousands of sensory hair cells are spread along an elongated membrane that acts as a spectral analyzer, with the result that each local group of hair cells responds best to a certain range of pitches, or sound frequencies. The hair cells then feed this information into afferent nerve fibers that carry the information to the brain.

Divergence from a common origin

Amniote vertebrates comprise three lineages of extant groups that diverged roughly 300 million years ago: the lepidosaurs, which include lizards and snakes; the archosaurs, which include crocodilians and birds; and mammals, which include egg-laying, pouched, and placental mammals. By comparing the skulls of the extinct common ancestors of these three lineages, as well as the ears of the most basal modern amniotes, researchers have concluded that ancestral amniotes had a small (perhaps less than 1 millimeter in length) but dedicated hearing organ: a sensory epithelium called a basilar papilla, with perhaps a few hundred sensory hair cells supported by a thin basilar membrane that is freely suspended in fluid. These rudimentary structures evolved from the hair cells of vestibular organs, which help organisms maintain their balance by responding to physical input, such as head rotation or gravity. Initially, the hearing organ only responded to low-frequency sounds. On their apical surface, all hair cells have tight tufts or bundles of large, hairlike villi known as stereovilli (or, more commonly stereocilia, even though they are not true cilia), which give hair cells their name. Between these stereovilli are proteinaceous links, most of which are closely coupled to sensory transduction channels that respond to a tilting of the stereovilli bundles caused by sound waves.

The amniote hearing organ evolved as a separate group of hair cells that lay between two existing vestibular epithelia. Low-frequency vestibular hair cells became specialized to transduce higher frequencies, requiring much faster response rates. This change is attributable in part to modifications in the ion channels of the cell membrane, such that each cell is “electrically tuned” to a particular frequency, a phenomenon still observed in some modern amniote ears. Moreover, the early evolution of these dedicated auditory organs in land vertebrates led to the loss of the heavy otolithic membrane that overlies the hair-cell bundles of vestibular organs and is responsible for their slow responses. What remains is the watery macromolecular gel known as the tectorial membrane, which assures that local groups of hair cells move synchronously, resulting in greater sensitivity.

Good high-frequency hearing did not exist from the start, however. For a period of at least 50 million years after amniotes arose, the three main lineages were most likely quite hard of hearing. They had not yet evolved any mechanism for absorbing sound energy from air; they lacked the middle ear and eardrum that are vital for the function of modern hearing organs. As such, ancestral amniotes most likely perceived only sounds of relatively low frequency and high amplitude that reached the inner ear via the limbs or, if the skull were rested on the ground, through the tissues of the head. It is unclear what kind of stimuli could have existed that would have led to the retention of such hearing organs for such a long time.

The magnificent middle ear

CONVERGING ON THE EAR: Starting around 250 million years ago, the three amniote lineages—lepidosaurs (lizards and snakes), archosaurs (crocodilians and birds), and mammals—separately evolved a tympanic middle ear, followed by evolution of the inner ear, both of which served to increase hearing sensitivity. Despite the independent origin of hearing structures in the three lineages, the outcomes were functionally quite similar, serving as a remarkable example of convergent evolution.
See full infographic: JPGILLUSTRATIONS: PHEBE LI FOR THE SCIENTIST. ICONS: ISTOCK.COMDuring the Triassic period, some 250 to 200 million years ago, a truly remarkable thing happened. Independently, but within just 20 million to 30 million years of one another, all three amniote lineages evolved a tympanic middle ear from parts of the skull and the jaws.²

The tympanic middle ear is the assemblage of tiny bones that connects at one end to an eardrum and at the other end to the oval window, an aperture in the bone of the inner ear. Despite the temporal coincidence in the evolution of these structures in the three amniote lineages and the functional similarities of the adaptations, the groups were by this time so far separated that the middle ears evolved from different structures into two different configurations. The single middle-ear bone, the columella, of archosaurs and lepidosaurs derived from the hyomandibular, a bone that earlier had formed a large strut connecting the braincase to the outer skull. In modern representatives, the columella is long and thin, with several, usually cartilaginous extensions known as the extracolumella. One of these, the “inferior process,” connects the inner surface of the eardrum and the columella, which then connects to the footplate that covers the oval window of the inner ear. This two-part system forms a lever that, together with the pressure increase incurred by transmitting from the much larger eardrum to the footplate, greatly magnifies sound entering the inner ear.

Inner-ear evolution

PITCH PERFECT: The hearing organs of amniotes are organized tonotopically, with hair cells sensitive to high frequencies at the basal end of the papilla, grading into low-frequency hair cells at the apical end.BASED ON MED-EL WWW.MEDEL.COMThe evolution of tympanic middle ears kick-started the evolution of modern inner ears, where sound waves are converted into the electrical signals that are sent to the brain. The inner ear is least developed in the lepidosaurs, most of which retained a relatively small auditory papilla, in some just a few hundred micrometers long. Many lepidosaurs, predominantly diurnal species, also lost their eardrum. Snakes reduced their middle ear, limiting their hearing to frequencies less than 1 kHz, about two octaves above middle C. (For comparison, humans can hear sounds up to about 15 or 16 kHz.) Clearly, hearing was not under strong selective pressure in this group. There are a few exceptions, however. In geckos, for example, which are largely nocturnal, the papillar structure shows unique specializations, accompanied by high sensitivity and strong frequency selectivity. Indeed, the frequency selectivity of gecko auditory nerve fibers exceeds that of many mammals.

One part of the inner ear that did improve in lizards (but not in snakes) is the hair cells, with the papillae developing different areas occupied by two structural types of these sound-responsive cells. One of these hair cell groups responds to sounds below 1 kHz and perhaps corresponds to the ancestral version. The higher-frequency hair cells have a more specialized structure, particularly with regard to the size and height of the stereovilli, with bundle heights and stereovillus numbers varying consistently along the papilla’s length. Taller bundles with fewer stereovilli, which are much less stiff and therefore respond best to low frequencies, are found at one end of the membrane, while shorter, thicker bundles with more stereovilli that respond best to higher frequencies are found at the other end—a frequency distribution known as a tonotopic organization. Still, with the exception of one group of geckos, lizard hearing is limited to below 5 to 8 kHz.

Amplification within the ear

HAIRS OF THE EAR: Rows of inner-ear hair cells have villous bundles (blue) on their apical surface that convert sound waves to nervous signals sent to the brain.© STEVE GSCHMEISSNER/SCIENCE SOURCEIn addition to the specialized structures of the middle and inner ears of amniotes that served to greatly increase hearing sensitivity, the hair cells themselves can produce active movements that further amplify sound stimuli. The evolutionarily oldest such active mechanism was discovered in the late 1980s by Jim Hudspeth’s group, then at the University of California, San Francisco, School of Medicine, working with frogs,⁵ and Andrew Crawford and Robert Fettiplace, then at the University of Cambridge, working with turtles.⁶ The amplification mechanism, called the active bundle mechanism, probably evolved in the ancestors of vertebrates and helped overcome the viscous forces of the surrounding fluids, which resist movement. When sound stimuli move the hair-cell bundle and thus open transduction channels to admit potassium ions, some calcium ions also enter the cell. These calcium ions bind to and influence the open transduction channels, increasing the speed with which these channels close. Such closing forces are exerted in phase with the incoming sound waves, increasing the distance that the hair cells move in response, and thereby increasing their sensitivity. It is likely that this mechanism operates in all vertebrate hair cells.⁵ In lizards, my group provided evidence that this bundle mechanism really does operate in the living animal.⁷

In 1986, a second mechanism of hair cell–driven sound amplification was discovered in mammalian OHCs by Bill Brownell’s group, then at the University of Florida School of Medicine. Brownell and his colleagues showed that mammalian OHCs, but not IHCs, changed their length very rapidly in phase with the signal if exposed to an alternating electrical field.⁸ Such fields occur when hair cells respond to sound. Subsequent experiments showed that the change in cell length is due to changes in the molecular configuration of a protein, later named prestin, which occurs in high density along the lateral cell membrane of OHCs. In mammals, the force produced by the OHCs is so strong that the entire organ of Corti, which includes all cell types that surround the hair cells and the basilar membrane itself, is driven in an up-and-down motion. This movement can amplify sounds by at least 40dB, allowing very quiet noises to be detected. There is evidence for the independent evolution of specific molecular configurations of prestins that allow for the amplification of very high ultrasonic frequencies in bats and whales.⁹

Bird ears also appear to produce active forces that amplify sound. The SHCs have bundles comprising up to 300 stereovilli (about three times as many as the bundles of mammalian OHCs),¹⁰ and the movement of these bundles probably drives the movement of THCs indirectly via the tectorial membrane. Also, very recent data from the lab of Fettiplace, now at the University of Wisconsin–Madison, suggests that in birds, prestin (albeit in a different molecular form) may work in the plane across the hearing organ (i.e., not up and down as in mammals), perhaps reinforcing the influence of the bundle active mechanism on the THCs via the tectorial membrane.¹¹

Three hundred million years of evolution have resulted in a fascinating variety of ear configurations that, despite their struc­tural diversity, show remarkably similar physiological responses.