A Fin is a Limb is a Wing

How Evolution Fashioned its Masterworks

By Carl Zimmer

The father of evolution was a nervous parent. Few things worried Charles Darwin more than the challenge of explaining how nature's most complex structures, such as the eye, came to be. "The eye to this day gives me a cold shudder," he wrote to a friend in 1860.

Today biologists are beginning to understand the origins of life's complexity—the exquisite optical mechanism of the eye, the masterly engineering of the arm, the architecture of a flower or a feather, the choreography that allows trillions of cells to cooperate in a single organism.

The fundamental answer is clear: In one way or another, all these wonders evolved. "The basic idea of evolution is so elegant, so beautiful, so simple," says Howard Berg, a Harvard researcher who has spent much of the past 40 years studying one of the humbler examples of nature's complexity, the spinning tail of common bacteria. "The idea is simply that you fiddle around and you change something and then you ask, Does it improve my survival or not? And if it doesn't, then those individuals die and that idea goes away. And if it does, then those individuals succeed, and you keep fiddling around, improving. It's an enormously powerful technique."

But nearly 150 years after Darwin first brought this elegant idea to the world's attention when he published The Origin of Species, the evolution of complex structures can still be hard to accept. Most of us can envision natural selection tweaking a simple trait—making an animal furrier, for example, or its neck longer. Yet it's harder to picture evolution producing a new complex organ, complete with all its precisely interlocking parts. Creationists claim that life is so complex that it could not have evolved. They often cite the virtuoso engineering of the bacterial tail, which resembles a tiny electric motor spinning a shaft, to argue that such complexity must be the direct product of "intelligent design" by a superior being.

The vast majority of biologists do not share this belief. Studying how complex structures came to be is one of the most exciting frontiers in evolutionary biology, with clues coming at remarkable speed.

Some have emerged from spectacular fossils that reveal the precursors of complex organs such as limbs or feathers. Others come from laboratories, where scientists are studying the genes that turn featureless embryos into mature organisms. By comparing the genes that build bodies in different species, they've found evidence that structures as seemingly different as the eyes of a fly and a human being actually have a shared heritage.

Scientists still have a long way to go in understanding the evolution of complexity, which isn't surprising since many of life's devices evolved hundreds of millions of years ago. Nevertheless, new discoveries are revealing the steps by which complex structures developed from simple beginnings. Through it all, scientists keep rediscovering a few key rules. One is that a complex structure can evolve through a series of simpler intermediates. Another is that nature is thrifty, modifying old genes for new uses and even reusing the same genes in new ways, to build something more elaborate.

Sean Carroll, a biologist at the University of Wisconsin–Madison, likens the body-building genes to construction workers. "If you walked past a construction site at 6 p.m. every day, you'd say, Wow, it's a miracle—the building is building itself. But if you sat there all day and saw the workers and the tools, you'd understand how it was put together. We can now see the workers and the machinery. And the same machinery and workers can build any structure."

A limb, a feather, or a flower is a marvel, but not a miracle.

From One Cell to Trillions

In every human body roughly ten trillion cells—brainless units of life—come together to work as a unified whole. "It's a complex dance," says Nicole King, a biologist at the University of California, Berkeley, requiring organization and constant communication. And it began more than 600 million years ago when organisms containing just one cell gave rise to the first multicellular animals, the group that now includes creatures as diverse as sea sponges, beetles, and us. It turns out that some of those single-celled ancestors were already equipped for social life.

King studies some of our closest living single-celled relatives, known as choanoflagellates. Choanoflagellates are easy to find. Just scoop some water from a local creek or marsh, put a few drops under a microscope, and you may see the tadpole-shaped creatures flitting about. You can tell them apart from other protozoans by a distinctive collar at the base of their tail.

When King and her colleagues examined the proteins made by choanoflagellates, they found several that were thought to be unique to animals—molecules essential to maintaining a multicellular body. "It really blew our minds," says King. "What are these single-celled organisms doing with these proteins?"

Some of the proteins normally create what King calls "an armlock between cells," keeping animal cells from sticking together randomly. King and her colleagues are running experiments to figure out how choanoflagellates use these adhesive proteins—perhaps to snag bacteria for food. Others play a role in cell-to-cell communication. Choanoflagellates, which presumably have no need to talk to other cells, may use these proteins to sense changes in their environment.

The discoveries suggest that many of the tools necessary to build a multicellular body already existed in our single-celled ancestors. Evolution borrowed those tools for a new task: building bodies of increasing complexity.

Blueprints for Bodies

A developing fly larva looks as featureless as a grain of rice. But it already bears a map of the complex creature it will become. Across the larva, different combinations of genes are active, marking it off into invisible compartments. These genes turn on other genes that give each compartment its shape and function: Some sprout legs, others wings, others antennae. An invisible anatomy becomes visible.

Flies aren't the only animals that build their bodies this way. Scientists have found that the genes responsible for laying out the fly's body plan have nearly identical counterparts in many other animals, ranging from crabs to earthworms to lampreys to us. The discovery came as a surprise, since these animals have such different-looking bodies. But now scientists generally agree that the common ancestor of all these animals—a wormlike creature that lived an estimated 570 million years ago—already had a basic set of body-plan genes. Its descendants then used those genes to build new kinds of bodies.

To appreciate how this tool kit can generate complexity, consider the velvet worm. The velvet worm creeps along the floors of tropical forests on nearly identical pad-shaped legs. It is, frankly, a boring little creature. Yet it is also the closest living relative to the single most diverse group of animals, the arthropods. Among arthropods, you can find a dizzying range of complex bodies, from butterflies to tarantulas, horseshoe crabs, ticks, and lobsters.

Scientists studying body-plan genes think arthropods started out much like velvet worms, using the same basic set of body-building genes to lay out their anatomy. Over time, copies of those genes began to be borrowed for new jobs. The invisible map of the arthropod body plan became more complex, with more compartments and new body parts sprouting from them.

Some compartments, for example, developed organs for breathing; later, in insects, those breathing organs evolved into wings. Early insect fossils preserve wings sprouting from many segments. Over time, insects shut off the wing-building genes in all but a few segments—or used some of the same genes to build new structures. Flies, for example, have just one pair of wings; a second pair has turned into club-shaped structures called halteres, which help flies stay balanced in flight.

"The segments have all become different, the appendages have all become different, but the machinery for making appendages is the same," says Sean Carroll. "Evolution is a tinkerer, an improviser."

How We Got a Head

The human head is, inch for inch, the most complex part of our body. Not only does it contain our brain, but it also packs in most of our sense organs: eyes, ears, a nose, and a tongue. The intricate bones of the skull add to the head's complexity, from the cranium that keeps the brain safe to the jaws that allow us to eat. Thousands of variations on the theme exist—think of hammerhead sharks, of anteaters, of toucans.

All those heads become even more remarkable when you look at two simple sea creatures that are the closest living relatives of the vertebrates (animals with backbones). These humble organisms have no heads at all. But they have the makings of one in their genes.

The larvacean, a tiny gelatinous tadpole, lives in a floating house it builds with its own mucus. Its nervous system, such as it is, is organized around a simple nerve cord running along its back. Even stranger is its cousin, the sea squirt. It starts out as a swimming larva, with a rodlike stiffener in its tail. When it matures, it drives its front end into the ocean floor, eats most of its nervous system, and turns its body into a basket for filtering food particles.

At first glance, these creatures seem unlikely to hold any clues to the origin of the vertebrate head. But a close look at the front tip of larvaceans and larval sea squirts reveals a small brainlike organ where a vertebrate would have a head. "There are 360 neural cells there. Compared with the vertebrate brain, that's nothing," says William Jeffery, a biologist at the University of Maryland. Yet scientists have seen a strikingly familiar pattern in how that tiny cluster of cells develops. Some of the same genes that build our own brains are at work there, and in roughly the same areas—front, middle, and rear.

Jeffery and his colleagues have also found that sea squirts have what appear to be primitive cousins of neural crest cells—the kind of cells that build much of the head in the developing embryos of vertebrates. Like our own neural crest cells, the sea squirt's emerge along the back of the developing embryo and migrate through the body. But instead of making a skull, neurons, and other parts of the head, they turn into pigment cells, adding brilliant colors to sea squirt bodies.

Over half a billion years ago our own headless ancestors may have resembled these modest creatures, already equipped with genes and cells that would later sculpt the faces and brains that make us human.

Catching the Light

Charles Darwin was well acquainted with the exquisite construction of the eye—the way the lens is perfectly positioned to focus light onto the retina, the way the iris adjusts the amount of light that enters the eye. An eye, it seemed, would be useless if it were anything less than perfect. In The Origin of Species, Darwin wrote that the idea of natural selection producing the eye "seems, I freely confess, absurd in the highest degree."

Yet the eye is actually far from perfect. The retina is so loosely attached to the back of the eye in humans that a sharp punch to the head may be enough to detach it. Its light-gathering cells point inward, toward the brain, not out toward the light. And the optic nerve starts out in front of the retina and then plunges through it to go to the brain. The place where the optic nerve burrows through the retina becomes the eye's blind spot. Evolution, with all its blunders, made the eye; Darwin himself had no doubt about that. But how?

A full answer has to account for not just our own eye, but all the eyes in the animal kingdom. Not long ago, the evidence suggested that the eyes in different kinds of animals—insects, cats, and octopuses, for example—must have evolved independently, much as wings evolved independently in birds and bats. After all, the differences between, say, a human eye and a fly's are profound. Unlike the human eye with its single lens and retina, the fly's is made up of thousands of tiny columns, each capturing a tiny fraction of the insect's field of vision. And while we vertebrates capture light with cells known as ciliary photoreceptors (for their hairlike projections, called cilia), insects and other invertebrates use rhabdomeric photoreceptors, cells with distinctive folds.

In recent years, however, these differences became less stark as scientists examined the genes that build photoreceptors. Insects and humans use the same genes to tell cells in their embryos to turn into photoreceptors. And both kinds of photoreceptors snag light with molecules known as opsins.

These links suggested that photoreceptors in flies, humans, and most other animals all evolved from a single type of cell that eventually split into two new cell types. If so, some animals might carry both types of photoreceptors. And in 2004, scientists showed that rag worms, aquatic relatives of earthworms, have rhabdomeric photoreceptors in their eyes and ciliary photoreceptors hidden in their tiny brain, where they appear to sense light to set the rag worm's internal clock.

With such discoveries, a new picture of eye evolution is emerging. The common ancestor of most animals had a basic tool kit of genes for building organs that could detect light. These earliest eyes were probably much like those found today in little gelatinous sea creatures like salps: just pits lined with photoreceptor cells, adequate to sense light and tell its direction. Yet they were the handiwork of the same genes that build our own eyes, and they relied on the same light-sensing opsins.

Evolution then used those basic genes to fashion more sophisticated eyes, which eventually acquired a lens for turning light into an image. The lens too did not appear out of nothing. Lenses are made of transparent proteins called crystallins, which can bend light "like protein glass," as one scientist says. And crystallins, it turns out, existed well before evolution put them to work in the eye. They were just doing other jobs.

Scientists have discovered one crystallin, for example, in the central nervous system of sea squirts. Instead of making a lens, it is part of a gravity-sensing organ. A mutation may have caused cells in the early vertebrate eye to make the crystallin as well. There it turned out to do something new and extraordinarily useful: bring the world into focus.

Date: 2015-12-11; view: 983