Eyes, Part One: Opening Up the Russian Doll

(The first of a two-part post)

The eye has always had a special place in the study of evolution, and Darwin had a lot to do with that. He believed that natural selection could produce the complexity of nature, and to a nineteenth century naturalist, nothing seemed as complex as an eye, with its lens, cornea, retina, and other parts working together so exquisitely.The notion that natural selection could produce such an organ "seems, I freely confess, absurd in the highest possible degree," Darwin wrote in the Origin of Species.

For Darwin, the key word in that line was seems. He realized that if you look at the different sort of eyes out in the natural world, and consider the ways in which they could have evolved, the absurdity disappears. The objection that the human eye couldn’t possibly have evolved, he wrote, “can hardly be considered real.”

The more scientists study the eye, the more they recognize that Darwin was right. This is not to say that they know everything about how the eye evolved. Evolutionary biology is not an automatic answer machine that can instantly tell you every detail about how eyes–or any other organ–evolved. Instead, scientists study eyes of different animals, the proteins they are made of, and the genes that store their recipe. They come up with hypotheses about how evolution could have produced these results. Those hypotheses then point the way to new experiments. In this way, evolutionary biology is no different from geology or meteorology, or any other science that illuminates the natural world.

To be precise, I should say that scientists study the evolution of "the eye." There are millions of different eyes (and other light-detecting organs), each built by a different species from its own unique set of genes. Closely related animals tend to have similar eyes, because they descend from recent ancestors. Some scientists study how eyes can adapt over a few million years to the special circumstances of a particular species. Other scientists step a little further back, to look at how the different types of eyes have evolved from simpler precursors. And other scientists step even further back in time, to find clues about where those simpler precursors came from. In this post, I will move back through time through these different stages of eye evolution (a la Richard Dawkins’s The Ancestor’s Tale.)

Humans have what’s known as a camera eye. Light first passes through a cornea, which refracts the light. It then passes through a lens, which refracts the light further, so that it forms a focused image on the retina. We are primates, and so it’s not surprising that all other primates have a similar type of eye. But different primates have important differences in the shape of their eye. Nocturnal primates have wider, more curved corneas than primates that are active during the day. A wider cornea lets nocturnal primates make the most of the moonlight by allowing more of it into the eye. Primates active during the day benefit from small flat corneas probably because the lens can sit further forward in the eye, producing a sharper image. This arrangement doesn’t let as much light in, but during the daytime, that’s no great loss. Chris Kirk of the University of Texas analyzed primate eyes in the December 2004 issue of The Anatomical Record (he has posted the paper on his web site).

For the most part, nocturnal and diurnal primates fit the same patterns as other mammals. But monkeys and apes (including humans) turn out to have extremely small, flat corneas, even compared to other primates that are active in the daytime. Kirk argues that this particular group of primates (called anthropoids) has experienced natural selection that has produced even sharper vision than found in other mammals active in the daytime. Other aspecsts of the anthropoid eye also make it sharp, including its fovea, a small spot on the retina that’s incredibly dense with photoreceptors. In fact, anthropoids are matched only by raptors for their sharp vision. It’s possible that our ancestors evolved such sharp eyes for hunting insects; monkeys and apes are also extremely social animals, and they rely on their keen eyes to look at one another and pick up subtle cues in their faces. Our ability to make sophisticated tools may have been made possible by the evolution of tiny corneas.

Changing the shape of an eye requires changing the molecules that make it up. Molecular fine-tuning can also alter an eye’s ability to block out UV rays, to refract light at different angles, or to become more sensitive to different colors. Despite the fact that all vertebrates share the same basic eye plan, you can find a wide range of molecules inside them. Some are found only in fish, some only in lizards, some only in mammals.

How does one group of animals evolve one of these new molecules? One way is to borrow it. Joram Piatigorsky of the National Eye Institute and his colleagues have identified many of the molecules that make up the lens and cornea of humans and other animals. These molecules are practically identical to molecules found elsewhere in the body. Some are essential for the development of the head in an embryo. Others protect our cells from heat and other stress, others detoxify poisons that would otherwise build up in the blood.

Originally, the evidence indicates, many of the molecules found in eyes today were only produced in other parts of the body. But then, thanks to a mutation, the same gene began producing its molecule in the developing eye. It just so happened to have the physical properties that made it well suited to being in an eye. In later generations, natural selection favored mutations that made it work better in the eye.

But this new job in the eye may have posed a trade-off for the molecule’s original job. Further fine-tuning may have only been possible when the gene went through a particularly drastic (but common) mutation: it duplicated. Now one copy of the gene could adapt to the eye, while the other continued specializing in its original job. (I wrote an essay a couple years ago about some of Piatigorsky’s work in Natural History.)

Darwin didn’t know about gene sharing or gene duplication, but he still managed to make some important observations about how the human eye could have evolved from a simpler precursor. Early eyes might have been nothing more than a patch of photosensitive cells that could tell an animal if it was in light or shadow. If that patch then evolved into a pit, it might also have been able to detect the direction of the light. Gradually, the eye could have taken on new functions, until at last it could produce full-blown images. Even today, you can find these sorts of proto-eyes in flatworms and other animals.

The closest invertebrate relatives of vertebrates fit nicely into Darwin’s predictions. Amphioxus, which looks like a sardine with its head cut off, lacks a true brain or camera eyes. But the front end of its nerve cord is slightly swollen, and is built by many of the same genes that build a human brain. What’s more, they grow a pit lined with light-sensitive cells which they seem to use to navigate through the water. The genes that build this pit are nearly identical to the ones that build our own.

The fact that Aphioxus has such a simple precursor to the vertebrate eye might suggest that this organ evolved from scratch. Yet eyes can be found on many other animals–which was how Darwin first figured out what a precursor to the vertebrate eye might have looked like. Eyes can found in insects, squid, and many other animals. Did they evolve independently?

The answer is yes and no. In the 1990s, Walter Gehring of the University of Basel and his colleagues discovered an essential eye-building gene called Pax-6 that was shared by insects and humans. If he inserted the human version of the gene into a fly larva, he got fly eyes popping up all over the fly’s body. Gehring has proposed that Pax-6 is a master control gene, switching on an entire circuit of eye-building genes. In insects and in humans (and in all of the animals that share a common ancestor), this circuit builds eyes. But in each lineage, a different set of genes have been incorporated into this circuit, so that they can build eyes as different as the compound eye of an insect and the camera eye of a human.

The simplest explanation for so many animals sharing this same circuit is that they all inherited it from their common ancestor–a small worm-like creature known as a bilaterian that might have lived 570 million years ago. Exactly what sort of eye these genes produced in the Precambrian mists of time isn’t clear, though. And until last fall, another feature of the eye didn’t seem to fit this hypothesis: its photoreceptors. Invertebrate eyes and vertebrate eyes use different photoreceptors to sense light. But researchers have found that both kinds of photoreceptors grow on a humble animal known as a ragworm, which is believed to have branched off very early in the evolution of bilaterians. It’s possible that the ancestor of living bilaterians produced both kinds of photoreceptors. One kind was lost in the vertebrate lineage, and the other was lost in the lineage that led to insects and other invertebrates with full-blown eyes.

Yet eyes are not limited to bilaterians. Jellyfish belong to a branch of animals known as cnidarians that split off from the ancestors of bilaterians some 600 million years ago. Some species have simple photoreceptors, while others have full-blown camera-eyes hanging from their tentacles. Biologists want to know whether these eyes evolved independently, or share some of the ancestral toolkit that produced human eyes and fly eyes. One hint that they share a common heritage is the fact that some of the genes that jellyfish use to build eyes bear a striking similarity to Pax-6 and other genes that build bilaterian eyes. On the other hand, most cnidarians (such as sea aneomones and corals) don’t have eyes. What’s more, jellyfish eyes are pretty weird compared to bilaterian eyes–for one thing, they don’t wire up to a brain. The larvae of one species grow photoreceptors that don’t even connect to a neuron. The photoreceptors link instead to hair-like structures in the same cell. Presumably light triggers these cells to flail their hairs to make the larva swim.

In years to come, the search for the roots of eye evolution will push even further back in time. In a paper in press at the Journal of Heredity, Walter Gehring points out that the first component of animal eyes to have evolved was the photoreceptor–a molecule that could catch light and turn it into a signal. One model for the origin of animal photoreceptors comes from colonies of algae, many of which have "eyespots" that allow them to swim towards the light so that they can photosynthesize. Perhaps early animals lived in colonies as well and had similar eyespots. Later, these simple photoreceptors evolved pigments and other molecules that helped capture more light, and eventually became able to form images.

But Gehring also proposes a weird but compelling alternative: our ancestors stole their eyes. Many times over the course of evolution, organisms have been engulfed by larger organisms, and the two have become integrated into a single being. Our cells, for example, contain mitochondria that we rely on to generate energy; originally, these were free-living oxygen-consuming bacteria. Another important fusion took place over two billion years ago, when bacteria that could carry out photosynthesis were consumed by an amoebae-like host. The bacteria then became a structure called the chloroplast, which can be found today in trees and other plants, as well as various sorts of algae. Increidbly, some of these algae were engulfed by other algae, which also came to depend on the photosynthesis carried out by the bacteria. Gehring likens these organisms to Russian dolls, with the original bacteria nestled deep within other organisms.

It’s likely that before the bacteria were consumed again and again, they had already evolved a light-sensing molecule that helped them harness sunlight–perhaps by acting as a biological clock. The algae that devoured the bacteria may have retained the ability to sense light for the same purpose. Gehring points out that one group of these algae–dinoflagellates–have fused with corals, jellyfish, and other animals. It’s possible that early animals may have incorporated the genes for light-sensing in their own genomes. If he’s right, we gaze at the world with bacterial eyes.