The Middle Earthe Three Ear Bones

Mammals are very special. With hair and milk-producing glands, we can easily be distinguished from other creatures. It surprises most people to learn that some of the most distinctive traits of mammals lie inside the ear. The bones of the mammalian middle ear are like those of no other animal: mammals have three bones, whereas reptiles and amphibians have only one. Fish have none at all. Where did our middle ear bones come from?

Some anatomy: recall that our three middle ear bones are known as the malleus, incus, and stapes. As we've seen, each of these ear bones is derived from the gill arches: the stapes from the first arch, and the malleus and incus from the second arch. It is here that our story begins.

In 1837, the German anatomist Karl Reichert was looking at embryos of mammals and reptiles to understand how the skull forms. He followed the gill arches of different species to understand where they ended up in the various skulls. As he did this again and again, he found something that appeared not to make any sense: two of the ear bones in the mammals corresponded to pieces of the jaw in the reptiles. Reichert could not believe his eyes, and his monograph reveals his excitement. As he describes the ear-jaw comparison, his prose departs from the normally staid description of nineteenth-century anatomy to express shock, even wonderment, at this discovery. The conclusion was inescapable: the same gill arch that formed part of the jaw of a reptile formed ear bones in mammals. Reichert proposed a notion that even he could barely believe—that parts of the ears of mammals are the same thing as the jaws of reptiles. Things get more difficult when we realize that Reichert proposed this several decades before Darwin propounded his notion of a family tree for life. What does it mean to call structures in two different species "the same" without a notion of evolution?

Much later, in 1910 and 1912, the German anatomist Ernst Gaupp picked up on Reichert's work and published an exhaustive study on the embryology of mammalian ears. Gaupp provided more detail and, given the times, interpreted Reichert's work in an evolutionary framework. Gaupp's story went like this: the three middle ear bones reveal the tie between reptiles and mammals. The single bone in the reptilian middle ear is the same as the stapes of mammals; both are second-arch derivatives. The explosive bit of information, though, was that the two other middle ear bones of mammals—the malleus and the incus—evolved from bones set in the back of the reptilian jaw. If this was indeed the case, then the fossil record should show bones shifting from the jaw to the ear during the origin of mammals. The problem was that Gaupp worked only on living creatures and didn't fully appreciate the role that fossils could play in his theory.

Beginning in the 1840s a number of new kinds of fossil creatures were becoming known from discoveries in South Africa and Russia. Often abundantly preserved, whole skeletons of dog-size animals were being unearthed. As they were discovered, many of them were crated and shipped to Richard Owen in London for identification and analysis. Owen was struck that these creatures had a mélange of features. Parts of their skeleton looked reptile-like. Other parts, notably their teeth, looked like mammals. And these were not isolated finds. It turns out that these "mammal-like reptiles" were the most common skeletons being uncovered at many fossil sites. Not only were they very common, there were many kinds. In the years after Owen, these mammal-like reptiles became known from other parts of the world and from several different time periods in earth history. They formed a beautiful transitional series in the fossil record between reptile and mammal.

Until 1913, embryologists and paleontologists were working in isolation from one another. At this time, the American paleontologist W. K. Gregory, of the American Museum of Natural History, saw an important link between Gaupp's embryos and the African fossils. The most reptilian of the mammal-like reptiles had only a single bone in its middle ear; like other reptiles, it had a jaw composed of many bones. Something remarkable was revealed as Gregory looked at the successively more mammalian mammal-like reptiles, something that would have floored Reichert had he been alive: a continuum of forms showing beyond doubt that over time the bones at the back of the reptilian jaw got smaller and smaller, until they ultimately lay in the middle ear of mammals. The malleus and incus did indeed evolve from jawbones. What Reichert and Gaupp observed in embryos was buried in the fossil record all along, just waiting to be discovered.

Why would mammals need a three-boned middle ear? This little linkage forms a lever system that allows mammals to hear higher-frequency sounds than animals with a single middle ear bone. The origin of mammals involved not only new patterns of chewing, as we saw in Chapter 4, but new ways of hearing. In fact, this shift was accomplished not by evolving new bones per se, but by repurposing existing ones. Bones originally used by reptiles to chew evolved in mammals to assist in hearing.

So much for the malleus and incus. Where, though, does the stapes come from?

If I simply showed you an adult human and a shark, you would never guess that this tiny bone deep inside a human's ear is the same thing as a large rod in the upper jaw of a fish. Yet, developmentally, these bones are the same thing. The stapes is a second-arch bone, as is the corresponding bone in a shark and a fish—the hyomandibula. But the hyomandibula is not an ear bone; recall that fish and sharks do not have ears. In our aquatic cousins, this bone is a large rod that connects the upper jaw to the braincase. Despite the apparent differences in the function and shape of these bones, the similarities between the hyomandibula and the stapes extend even to the nerves that supply them The key nerve for the functioning of both bones is the second-arch nerve, the facial nerve. We thus have a situation where two very different bones have similar developmental origins and patterns of innervation. Is there an explanation for this?

Again, we look to the fossils. As we trace the hyomandibula from sharks to creatures like Tiktaalik to amphibians, we can see how it gets smaller and smaller, ultimately shifting position from the upper jaw to play a role in hearing. The name changes, too. When it is big and supporting the jaw, we call it a hyomandibula; when it is small and functions in hearing, it is known as a stapes. This shift happened when the descendants of fish began to walk on land. Hearing in water is different from hearing on land, and the small size and position of the stapes makes it ideal for picking up vibrations in air. The new ability came about by modifying the upper jawbone of a fish.

Fish Amphibian Reptile Mammal Brain

We can trace bones from gill arches to our ears, first during the transition from fish to amphibian (right), and later during the shift from reptile to mammal (left).

Our middle ear contains a record of two of the great transformations in the history of life. The origin of our stapes, and its transformation from a jaw support bone to an ear bone, began when fish started to walk on land. The other big event took place during the origin of mammals, when bones at the back of a reptile jaw became our malleus and incus.

Now let's go further inside the ear—to the inner ear.

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