Crystal balls: borrowed genes can help anything evolve—even the eye - The Evolutionary Front

Natural History, April, 2002 by Carl Zimmer

The eye to this day gives me a cold shudder," Charles Darwin once wrote to a friend. If his theory of evolution was everything he thought it was, a complex organ such as the eye could not lie beyond its reach. And no one appreciated the beautiful construction of the eye more than Darwin--from the way the lens was perfectly positioned to focus light onto the retina to the way the iris adjusted the amount of light that could enter the eye. In the Origin of Species, he wrote that the idea of natural selection producing the eye "seems, I freely confess, absurd in the highest possible degree."

But Darwin also knew that a cold shudder was not reason enough to abandon a scientific theory. He looked at the eyes of many different animals--from flatworms to crustaceans to vertebrates--and found among them a gradation of forms, from a simple patch of light-sensitive tissue all the way to an elaborate image-forming organ complete with lens, iris, and retina. He decided there was no reason that evolution could not have led gradually from one arrangement to another.

Darwin considered only the anatomy of the eye, because the biochemistry of vision was still a mystery in his day. Of course, an eye is far more than just what can be seen by another eye. All the work involved in vision--bending and catching light, fine-tuning the image that gets sent to the brain, keeping the eye clear and firm over the years--is carried out by an army of specialized molecules, produced in turn by specialized types of cells. And these cells contain genes and proteins that interact with one another in a dense web of cooperation and control, of feedback and inhibition. If Darwin could have seen the molecular complexity of the eye, his shudder might well have turned even colder.

But before too long, the shudder would fade. As scientists have uncovered the biochemical intricacies of the eye, they've also made great strides in understanding how it has evolved. In the process, they've come face-to-face with evolution's remarkable laziness. Instead of giving rise to entirely new genes, evolution has in many cases simply borrowed old ones.

The story of this discovery begins in the 1960s, when scientists started to study the molecules that make up one important part of the vertebrate eye, the lens. The lens is essentially a blob of clear skin cells. As an embryo develops, a patch of cells on each side of its head begins to differentiate from the surrounding tissue. These cells start producing protein molecules called crystallins, which make up 90 percent of the protein in the lens. Soon the cells become little more than bags of crystallin.

Thanks to their structure, crystallins make a lens act as if it were made of glass. They bend the light as it passes through, and because they pack tightly together in an orderly way, rather than sticking together in irregular clumps, they don't scatter the rays randomly. Crystallins are also incredibly tough--and they need to be, because they can't be replaced once they've been formed. They are the longest-lived proteins in the body; many of the crystallins in the eyes of a centenarian were there when he or she was an embryo. If they become damaged and start clumping together, cataracts form.

When scientists first began investigating various vertebrate lenses, they expected to find at most just a few kinds of crystallins. Other molecules that carry out equally specialized jobs--light-sensitive rhodopsin in the retina, for example, and oxygen-ferrying hemoglobin in red blood cells--are pretty much identical in any vertebrate you care to examine, from a parrot to a python. But by the 1970s it became evident that crystallins are unusual in this respect: they come in a surprising variety of different structures, each of which interacts with light in a unique way. And the different crystallins are not mixed together randomly; as the lens grows, it builds up rings like an onion, and each new ring is made up of distinctive proportions of the various crystallins. These different combinations give each ring the ability to bend light at a particular angle. As a result, the entire lens can focus light onto a small spot on the retina.

But an even bigger surprise was in store for researchers. It turns out that certain vertebrates possess unique types of crystallins, present in no other eyes. Birds and reptiles, for example, all have lens proteins (dubbed delta-crystallins) that mammals and amphibians lack. Amphibians have crystallins of their own, as do mammals. These discoveries hinted that the vertebrate eye has had a turbulent evolutionary history.

The fossil record suggests that the first full-blown vertebrate eye arose 530 million years ago in a primitive fish. As the fish's descendants diverged into new forms, new crystallins evolved in their eyes. Birds and reptiles, for example, descend from a common ancestor that lived about 300 million years ago--an ancestor that amphibians and mammals do not share--and this ancient creature presumably evolved delta-crystallins and passed them on to its descendants. New crystallins did not simply evolve as minor variations on old ones, however. Biologists can group the proteins into distinct "families," and these families bear little resemblance to one another. Somehow, evolution devised transparent proteins again and again.