Page 12 - Spring 2018

Physics and the Mammalian Ear
3B) and that later in its evolution, three ossicles were better than one at transmitting high-frequency sounds.
It was serendipitous that at the time of the origin of the middle ear, mammalian ancestors were changing the way they obtained and processed food in the mouth, partly by developing a new and unique jaw joint (Manley, 2010). This process resulted in the gradual loss of bones from the old jaw joint, bones that happened to lie between the skin just behind the lower jaw and the stapes that was connected to the bone surrounding the inner ear. The redundant jaw bones were co-opted into the mammalian middle ear, which arose independently of and at a different bodily location to that of nonmammalian land vertebrates and, indeed, inde- pendently in egg-laying and live-bearing mammals (Manley, 2010). Mammalian groups thus share a sensory architecture that arose from a common ancestry and, therefore, a com- mon genetic substrate that is characteristic for mammals. The physics of the result of that evolutionary event is in al- most all respects, especially regarding impedance matching between the medium of air and the medium of the inner ear fluids, not unique but fully comparable to that of nonmam- mals (Manley, 1995).
Significantly, the middle ear of nonmammals such as birds evolved completely independently using a single element (of the same origin as, i.e., homologous to, the stapes; Fig- ure 3, A and C) that became attached to an eardrum using new, flexible cartilage elements that also form a lever system. Both these middle ear systems thus do not represent physical systems whose structure represents some idealized “design” but are the result of the contingencies of their histories that determined the elements that were “accidentally” available. These parallel evolutionary processes in mammals and non- mammals are due to the requirements of detecting the same physical modality. Long after middle ears arose, the inner ear of mammals evolved the ability to detect high frequen- cies because their middle ear can transmit such frequencies. The fact that the functions of one- and three-ossicle middle ears are extremely similar in the frequency range below 10 kHz nonetheless testifies to both the creative nature and the importance of history in the evolutionary selection process.
Modern Vertebrate Groups and
Their Hearing Organs Did Not Arise
in a Linear Sequence
A common mistake among nonbiologists (e.g., Lorimer et al., 2015) is to represent the evolution of modern vertebrates as a staircase, which implies that in their evolution, includ-
10 | Acoustics Today | Spring 2018
Figure 3. Middle ear configurations and function. A: nonmamma- lian, single-ossicle type of middle ear. B: mammalian, three-ossicle type of middle ear. In A and B, the inner ear (not shown) is to the left and connected via the footplate (Fp) that is seated in the wall of the inner ear. T, tympanic membrane or eardrum; EC, extracolu- mella (gray); Col, columella = stapes (St); Mal, malleus; Inc, Incus. C: schematic representation of the columellar-type middle ear. Compare with lever systems shown at bottom right that illustrate the mode of operation. In each case, air particle velocity over the eardrum and centered at P1 (red arrow) provides the eardrum with an oscilla- tory movement. The fulcrum at R (green) leads to a higher oscillating pressure (P2) on the columella (blue arrow). Bottom right: equiva- lent lever systems for the three-ossicle mammalian middle ear. From Manley (2017), with permission.
ing that of their hearing organs, the different modern groups represent a series of steps or a sequence of refinements lead- ing gradually to the supposedly final improvement seen in mammals. In fact, all organs of extant land vertebrates, whether reptiles, birds, or mammals, evolved fully indepen- dently of each other, yet all originated from the same, very simple, ancestral form in the earliest reptiles (Manley and Ladher, 2008; Figure 4). There is, therefore, no reason what- soever to expect that mammalian auditory organs should be the best or most sophisticated. Depending on the evolu- tionary pressures, which were determined by environmental strategy, predator-prey relationships, and requirements for conspecific communications, each extant group of verte- brates has found an adequate hearing solution. Acute sen- sitivity and sharp frequency resolution, features of hearing organs frequently associated with mammals, have evolved independently in all groups of modern land vertebrates. In- deed, the auditory nerve fibers of some lizards are among the most sharply frequency tuned of any vertebrates, including those of most mammals (Manley, 2001). Auditory sensitivity in birds of prey, especially those (such as barn owls) that rely