Your Inner Fish: A Journey Into the 3.5-Billion-Year History of the Human Body

by Neil Shubin

  The reptile Bill had found was a tritheledont, a creature known from South Africa as well as now from Nova Scotia. These were very rare, so we wanted to return to Nova Scotia the next summer to find more. I spent the whole winter tense with anticipation. If I could have chipped through the winter ice to find fossils, I would have done it.

  In the summer of 1985, we returned to the site where we had found the tritheledont. The fossil bed was just at beach level, where a little piece of the cliff had fallen off several years before. We had to time our daily visit just so: the site was inaccessible at high tide because the water came up too high around a point we had to navigate. I’ll never forget that first day of excitement when we rounded the point to find our little patch of bright orange rock. The experience was memorable for what was missing: most of the area we had worked the year before. It had weathered away the previous winter. Our lovely fossil site, containing beautiful tritheledonts, was gone with the tides.

  The good news, if you could call it that, was that there was a little more orange sandstone to scan along the beach. Most of the beach, in particular the point we had to go around each morning, was made up of basalt from a 200-million-year-old lava flow. We were positive no fossils could be found there, for it is virtually axiomatic that these rocks, which were once super hot, would never preserve fossil bone. We spent five or more days timing our visits to the sites by the tides, pawing away at the orange sandstones beyond it, and finding absolutely nothing.

  Our breakthrough came when the president of the local Lions Club came by our cabin one night looking for judges for the local beauty contest, to crown Parrsboro’s Miss Old Home Week. The town always relied on visitors for this onerous task, because internecine passions typically run high during the event. The usual judges, an elderly couple from Quebec, were not visiting this year, and the crew and I were invited to substitute.

  But in judging the beauty contest and arguing over its conclusion, we stayed up way too late, forgot about the next morning’s tides, and ended up trapped around a bend in the basalt cliffs. For about two hours, we were stuck on a little promontory about fifty feet wide. The rock was volcanic and not the type one would ever choose to search for fossils. We skipped stones until we got bored, then we looked at the rocks: maybe we’d find interesting crystals or minerals. Bill disappeared around a corner, and I looked at some of the basalt behind us. After about fifteen minutes I heard my name. I’ll never forget Bill’s understated tone: “Uh, Neil, you might want to come over here.” As I rounded the corner, I saw the excitement in Bill’s eyes. Then I saw the rocks at his feet. Sticking out of the rocks were small white fragments. Fossil bones, thousands of them.

  This was exactly what we were looking for, a site with small bones. It turned out that the volcanic rocks were not entirely volcanic: slivers of sandstone cut through the cliff. The rocks had been produced by an ancient mudflow associated with a volcanic eruption. The fossils were stuck in the ancient muds.

  We brought tons of these rocks home. Inside were more tritheledonts, some primitive crocodiles, and other lizard-like reptiles. The tritheledonts were the gems, of course, because they showed that some kinds of reptiles already displayed our mammalian kind of chewing.

  Early mammals, such as those Farish’s team uncovered in Arizona, had very precise patterns of biting. Scrapes on the cusps of an upper tooth fit against mirror images of these scrapes on a lower tooth. These patterns of wear are so fine that different species of early mammals can be distinguished by their patterns of tooth wear and occlusion. Farish’s Arizona mammals have a different pattern of cusps and chewing than those of the same age from South America, Europe, or China. If all we had to compare these fossils to were living reptiles, then the origin of mammalian feeding would appear to be a big mystery. As I’ve mentioned, crocodiles and lizards do not have any kind of matching pattern of occlusion. Here is where creatures like tritheledonts come in. When we go back in time, to rocks about 10 million years older, such as those in Nova Scotia, we find tritheledonts with an incipient version of this way of chewing. In tritheledonts, individual cusps do not interlock in a precise way, as they do in mammals; instead, the entire inner surface of the upper tooth shears against the outer surface of the lower tooth, almost like a scissors. Of course, these changes in occlusion did not happen in a vacuum. It should come as no surprise that the earliest creatures to show a mammalian kind of chewing also display mammalian features of the lower jaw, skull, and skeleton.

  A tritheledont and a piece of its upper jaw discovered in Nova Scotia. Jaw fragment illustrated by Lazlo Meszoley.

  Because teeth preserve so well in the fossil record, we have very detailed information about how major patterns of chewing—and the ability to use new diets—arose over time. Much of the story of mammals is the story of new ways of processing food. Soon after we encounter tritheledonts in the fossil record, we start seeing all sorts of new mammal species with new kinds of teeth, as well as new ways of occluding and using them. By about 150 million years ago, in rocks from around the world, we find small rodent-size mammals with a new kind of tooth row, one that paved the way for our own existence. What made these creatures special was the complexity of their mouths: the jaw had different kinds of teeth set in it. The mouth developed a kind of division of labor. Incisors in the front became specialized to cut food, canines further back to puncture it, and molars in the extreme back to shear or mash it. These little mammals, which resemble mice, have a fundamental piece of our history inside of them. If you doubt this, imagine eating an apple lacking your incisor teeth or, better yet, a large carrot with no molars. Our diverse diet, ranging from fruit to meat to Twinkie, is possible only because our distant mammalian ancestors developed a mouth with different kinds of teeth that can occlude precisely. And yes, initial stages of this are seen in tritheledonts and other ancient relatives: the teeth in the front have a different pattern of blades and cusps than those in the back.

  TEETH AND BONES—THE HARD STUFF

  It almost goes without saying that what makes teeth special among organs is their hardness. Teeth have to be harder than the bits of food they break down; imagine trying to cut a steak with a sponge. In many ways, teeth are as hard as rocks, and the reason is that they contain a crystal molecule on the inside. That molecule, known as hydroxyapatite, impregnates the molecular and cellular infrastructure of both teeth and bones, making them resistant to bending, compression, and other stresses. Teeth are extra hard because their outer layer, enamel, is far richer in hydroxyapatite than any other structure in the body, including bone. Enamel gives teeth their white sheen. Of course, enamel is only one of the layers that make up our teeth. The inner layers, such as the pulp and dentine, are also filled with hydroxyapatite.

  There are lots of creatures with hard tissues—clams and lobsters, for example. But they do not use hydroxyapatite; lobsters and clams use other materials, such as calcium carbonate or chitin. Also, unlike us, these animals have an exoskeleton covering the body. Our hardness lies within.

  Our particular brand of hardness, with teeth inside our mouths and bones inside our bodies, is an essential part of who we are. We can eat, move about, breathe, even metabolize certain minerals because of our hydroxyapatite-containing tissues. For these capabilities, we can thank the common ancestor we share with all fish. Every fish, amphibian, reptile, bird, and mammal on the planet is like us. All of them have hydroxyapatite-containing structures. But where did this all come from?

  There is an important intellectual issue at stake here. By knowing where, when, and how hard bones and teeth came about, we will be in a position to understand why. Why did our kind of hard tissues arise? Did they come about to protect animals from their environment? Did they come about to help them move? Answers to these questions lie in the fossil record, in rocks approximately 500 million years old.

  Some of the most common fossils in ancient oceans, 500 million to 250 million years old, are conodonts. Conodonts were discovered in the 1830s
by the Russian biologist Christian Pander, who will reappear in a few chapters. They are small shelly organisms with a series of spikes projecting out of them. Since Pander’s time, conodonts have been discovered on every continent; there are places where you cannot crack a rock without finding vast numbers of them. Hundreds of kinds of conodonts are known.

  For a long time, conodonts were enigmas: scientists disagreed over whether they were animal, vegetable, or mineral. Everybody seemed to have a pet theory. Conodonts were claimed to be pieces of clams, sponges, vertebrates, even worms. The speculation ended when whole animals started to show up in the fossil record.

  The first specimen that made sense of everything was found by a professor of paleontology rummaging through the basement at the University of Edinburgh: there was a slab of rock with what looked like a lamprey in it. You might recall lampreys from biology class—these are very primitive fish that have no jaws. They make their living by attaching to other fish and feeding on their bodily fluids. Embedded in the front of the lamprey impression were small fossils that looked strangely familiar. Conodonts. Other lamprey-like fossils started to come out of rocks in South Africa and later the western United States. These creatures all had an exceptional trait: they had whole assemblages of conodonts in their mouths. The conclusion became abundantly clear: conodonts were teeth. And not just any teeth. Conodonts were the teeth of an ancient jawless fish.

  We had the earliest teeth in the fossil record for over 150 years before we realized what they were. The reason comes down to how fossils are preserved. The hard bits, for example teeth, tend to get preserved easily. Soft parts, such as muscle, skin, and guts, usually decay without fossilizing. We have museum cabinets full of fossil skeletons, shells, and teeth, but precious few guts and brains. On the rare occasions when we find evidence of soft tissues, they are typically preserved only as impressions or casts. Our fossil record is loaded with conodont teeth, but it took us 150 years to find the bodies. There is something else remarkable about the bodies to which conodonts belonged. They have no hard bones. These were soft-bodied animals with hard teeth.

  For years, paleontologists have argued about why hard skeletons, those containing hydroxyapatite, arose in the first place. For those who believed that skeletons began with jaws, backbones, or body armor, conodonts provide an “inconvenient tooth,” if you will. The first hard hydroxyapatite-containing body parts were teeth. Hard bones arose not to protect animals, but to eat them. With this, the fish-eat-fish world really began in earnest. First, big fish ate little fish; then, an arms race began. Little fish developed armor, big fish obtained bigger jaws to crack the armor, and so on. Teeth and bones really changed the competitive landscape.

  Things get more interesting still as we look at some of the first animals with bony heads. As we move up in time from the earliest conodont animals, we see what the first bony-head skeletons looked like. They belonged to fish called ostracoderms, are about 500 million years old, and are found in rocks all over the world, from the Arctic to Bolivia. These fish look like hamburgers with fleshy tails.

  The head region of an ostracoderm is a big disk covered by a shield of bone, looking almost like armor. If I were to open a museum drawer and show you one, you would immediately notice something odd: the head skeleton is really shiny, much like our teeth or the scales of a fish.

  A conodont (left) and an ostracoderm (right). Conodonts were originally found isolated. Then, as whole animals became known, we learned that many of them functioned together as a tooth row in the mouths of these soft-bodied jawless fish. Ostracoderms have heads covered with a bony shield. The microscopic layers of that shield look like they are composed of little tooth-like structures. Conodont tooth row reconstruction courtesy of Dr. Mark Purnell, University of Leicester, and Dr. Philip Donoghue, University of Bristol.

  One of the joys of being a scientist is that the natural world has the power to amaze and surprise. Here, in ostracoderms, an obscure group of ancient jawless fish, lies a prime example. Ostracoderms are among the earliest creatures with bony heads. Cut the bone of the skull open, embed it in plastic, pop it under the microscope, and you do not find just any old tissue structure; rather, you find virtually the same structure as in our teeth. There is a layer of enamel and even a layer of pulp. The whole shield is made up of thousands of small teeth fused together. This bony skull—one of the earliest in the fossil record—is made entirely of little teeth. Teeth originally arose to bite creatures; later, a version of teeth was used in a new way to protect them.

  TEETH, GLANDS, AND FEATHERS

  Teeth not only herald a whole new way of living, they reveal the origin of a whole new way of making organs. Teeth develop by an interaction of two layers of tissue in our developing skin. Basically, two layers approach each other, cells divide, and the layers change shape and make proteins. The outer layer spits out the molecular precursors of enamel, the inner layer the dentine and pulp of the inside of the tooth. Over time, the structure of the tooth is laid down, then tweaked to make the patterns of cusps and troughs that distinguish each species.

  The key to tooth development is that an interaction between these two layers of tissue, an outer sheet of cells and an inner loose layer of cells, causes the tissue to fold and makes both layers secrete the molecules that build the organ. It turns out that exactly the same process underlies the development of all the structures that develop within skin: scales, hair, feathers, sweat glands, even mammary glands. In each case, two layers come together, fold, and secrete proteins. Indeed, the batteries of the major genetic switches that are active in this process in each kind of tissue are largely similar.

  Teeth, breasts, feathers, and hair all develop from the interactions between layers of skin.

  This example is akin to making a new factory or assembly process. Once plastic injection was invented, it was used in making everything from car parts to yo-yos. Teeth are no different. Once the process that makes teeth came into being, it was modified to make the diverse kinds of organs that lie within skin. We saw this taken to a very great extreme in the ostracoderms. Birds, reptiles, and humans are just as extreme in many ways. We would never have scales, feathers, or breasts if we didn’t have teeth in the first place. The developmental tools that make teeth have been repurposed to make other important skin structures. In a very real sense organs as different as teeth, feathers, and breasts are inextricably linked by history.

  A theme of these first four chapters is how we can trace the same organ in different creatures. In Chapter 1 we saw that we can make predictions and find versions of our organs in ancient rocks. In Chapter 2 we saw how we can trace similar bones all the way from fish to humans. Chapter 3 shows how the real heritable part of our bodies—the DNA and genetic recipe that builds organs—can be followed in very different creatures. Here, in teeth, mammary glands, and feathers, we find a similar theme. The biological processes that make these different organs are versions of the same thing. When you see these deep similarities among different organs and bodies, you begin to recognize that the diverse inhabitants of our world are just variations on a theme.

  CHAPTER FIVE

  GETTING AHEAD

  It was two nights before my anatomy final and I was in the lab at around two in the morning, memorizing the cranial nerves. There are twelve cranial nerves, each branching to take bizarre twists and turns through the inside of the skull. To study them, we bisected the skull from forehead to chin and sawed open some of the bones of the cheek. So there I was, holding half of the head in each hand, tracing the twisted paths that the nerves take from our brains to the different muscles and sense organs inside.

  I was enraptured by two of the cranial nerves, the trigeminal and the facial. Their complicated pattern boiled down to something so simple, so outrageously easy that I saw the human head in a new way. That insight came from understanding the far simpler state of affairs in sharks. The elegance of my realization—though not its novelty; comparative anatomists had had it a century o
r more ago—and the pressure of the upcoming exam led me to forget where I was. At some point, I looked around. It was the middle of the night and I was alone in the lab. I also happened to be surrounded by the bodies of twenty-five human beings under sheets. For the first and last time, I got the willies. I worked myself into such a lather that the hairs on the back of my neck rose, my feet did their job, and within a nanosecond I found myself at the bus stop, out of breath. It goes without saying that I felt ridiculous. I remember telling myself: Shubin, you’ve become hard-core. That thought did not last long; I soon discovered I had locked my house keys in the lab.

  What made me so hard-core is that head anatomy is deeply mesmerizing, in fact, beautiful. One of the joys of science is that, on occasion, we see a pattern that reveals the order in what initially seems chaotic. A jumble becomes part of a simple plan, and you feel you are seeing right through something to find its essence. This chapter is about seeing that essence inside our own heads. And, of course, the heads of fish.

  THE INNER CHAOS OF THE HEAD

  Head anatomy is not only complicated but hard to see, since, unlike other parts of the body, the tissues of the head are encapsulated in a bony box. We literally have to saw through the cheek, forehead, and cranium to see the vessels and organs. Having thus opened a human head, we find a clump of what looks like tangled fishing lines. Vessels and nerves make curious loops and turns as they travel through the skull. Thousands of nerve branches, muscles, and bones sit within this small box. At first glance, the whole array is a bewildering mess.