Evo Edu Outreach (2008) 1:487–492 DOI 10.1007/s12052-008-0089-9 ORIGINAL SCIENTIFIC ARTICLE The Evolution of Extraordinary Eyes: The Cases of Flatfishes and Stalk-eyed Flies Carl Zimmer Published online: 16 October 2008 # Springer Science + Business Media, LLC 2008 The history of life is an unbroken stream of evolution glimpses of the gradations that appear to have occurred during stretching over 3.5 billion years. In order to study it—and eye evolution, and provide a scenario for the unseen steps that in order to describe it—it must be carved into episodes. If have led to the emergence of the vertebrate eye.” They end scientists want to understand the origin, say, of bats, they their review with the emergence of the vertebrate eye. Of do not run experiments to test a hypothesis about how DNA course, Lamb et al. (2007) do not mean to imply that the first evolved on the early Earth. They do not do research on evolution of vertebrate eyes ceased after they first emerged. the transition from single-celled protozoans to the first But their focus is not on what happened afterwards. animals 600 million years ago. Likewise, they do not get Figuring out how a patch of light-sensitive receptors bogged down with bat evolution after bats first evolved— evolved into a camera-like imaging system shared by how, for example, bats spread around the world and how 40,000-odd species of vertebrates is certainly an important they coevolved with their prey. There is only so much time thing to do, and it is a job that will fill many scientists’ in the day. Science writers follow the same rules to describe entire careers. But when the first full-blown vertebrate eyes evolution. A newspaper article on the evolution of bats emerged in some primitive fishes half a billion years ago, must focus only on that brief episode of life’s history. Let the evolution of the vertebrate eye did not stop. The eyes of its scope grow too large, and it will be too big for a book— every vertebrate alive today are different in some important or a shelf of books. ways from those early eyes. In some cases, the transforma- This simple necessity can, unfortunately, give people the tion has been exquisitely subtle. But in others, it has been wrong impression about evolution. We tend to picture so extreme as to be quite striking. evolution as a series of isolated milestones. Once some In this essay, I will look at two animals in which evolution particular trait evolves, we may assume that evolution has radically reworked a “standard” kind of eye: flatfishes and simply stops. stalk-eyed flies. In both cases, eyes have moved far from their The history of eyes is particularly vulnerable to this original position on the head. But flatfishes and stalk-eyed illusion. Consider, for example, a masterful paper entitled, flies are not just freakish codas on the symphony of evolution. “Evolution of the vertebrate eye: opsins, photoreceptors, Instead, they are remarkable illustrations of some of the most retina, and eye cup,” published by Trevor Lamb of powerful forces shaping all life, weird or otherwise. Australian National University and his colleagues in the Flatfishes—such as flounder, turbot, and plaice—are December 2007 issue of Nature Reviews Neuroscience among the most striking animals in the sea. They spend (Lamb et al. 2007). “Here,” Lamb and his co-authors much of their adult life sideways, hugging the sea floor announce, “we review a wide range of findings that capture where they lie in wait to ambush smaller fish. Their anatomy and DNA both reveal that they belong to the most diverse radiation of vertebrates today, known as the teleosts. Teleosts include most of the fishes we are most C. Zimmer (*) Guilford, CT, USA familiar with, such as goldfish and trout. In many respects, e-mail: [email protected] flatfishes have a standard teleost body plan. But as they 488 Evo Edu Outreach (2008) 1:487–492 have adapted to life on the sea floor, some new traits have fish could have evolved in a series of steps. He had read evolved. All vertebrates, ourselves included, use hair cells how young flatfishes—with normal eyes—sometimes fall in the inner ear to keep ourselves balanced. In most flatfish to the sea floor and then twist their lower eye upward to see species, the hairs have changed orientation to match the above them. They seem to strain their lower eye, twisting it orientation of their bodies. (Schrieber 2006). Many flat- as far as possible. fishes can camouflage the upward-facing side of their body. At this point in his life, Darwin was warming to Jean The underside is pale, and in many species the fin on the Lamarck, the French naturalist who had proposed an earlier underside is tiny. theory of evolution in 1800. Lamarck had argued that an And then, of course, there are the eyes. animal’s body changed through its experiences, and that On a typical teleost, such as a goldfish, the eyes face out those changes could be passed down to its offspring. from either side of the head. On a flounder, both eyes sit on Natural selection, Darwin’s great discovery, depended one side, gazing upwards. It takes time for this Picasso-esque instead on pure inheritance. Nothing we do in our lives anatomy to emerge: flatfishes are born with eyes in the changes the inherited traits we pass down to our offspring. normal position, but as they grow, one eye moves across its But Darwin struggled with the mystery of heredity. Over head to join its partner. To accommodate this migrant, the time, he became more open to Lamarck. And so he offered bones of the flatfish head twist and turn to make room. a surprisingly Lamarckian explanation of creeping flat- When Charles Darwin published the Origin of Species in fishes’ eyes. The more the young flatfishes strained their 1859, a number of critics took him on, but none more lower eyes, he suggested, the more it migrated during its seriously than a British zoologist named St. George Jackson development towards the other side. He wrote, Mivart. In 1871, Mivart published a full-scale challenge to We thus see that the first stages of the transit of the eye evolution by natural selection, called On the Genesis of from one side of the head to the other, which Mr. Species. In one of his attacks, Mivart wielded the flatfish: Mivart considers would be injurious, may be attributed In all these fishes the two eyes, which in the young are to the habit, no doubt beneficial to the individual and situated as usual one on each side, come to be placed, to the species, of endeavouring to look upward with in the adult, both on the same side of the head. If this both eyes, while resting on one side at the bottom. condition had appeared at once, if in the hypothetically (Darwin 1872) fortunate common ancestor of these fishes an eye had Natural selection had driven the eye further, Darwin suddenly become thus transferred, then the perpetua- proposed. “For all spontaneous variations in the right tion of such a transformation by the action of “Natural direction will thus be preserved; as will those individuals Selection” is conceivable enough. Such sudden which inherit in the highest degree the effects of the changes, however, are not those favoured by the increased and beneficial use of any part. How much to Darwinian theory, and indeed the accidental occur- attribute in each particular case to the effects of use, and how rence of such a spontaneous transformation is hardly much to natural selection, it seems impossible to decide.” conceivable. But if this is not so, if the transit was By the early 1900s, as scientists began to understand gradual, then how such transit of one eye a minute how genes work, they realized that mutations could fuel fraction of the journey towards the other side of the natural selection. But some biologists still argued that head could benefit the individual is indeed far from evolution might proceed by giant leaps. In the 1930s, the clear. It seems, even, that such an incipient transfor- German biologist Richard Goldschmidt pointed to rare mation must rather have been injurious. (Mivart 1871) cases in which animals were produced with dramatic How exactly a transitional flatfish eye would have hurt changes to their bodies. He called them “hopeful monsters,” the animal, Mivart did not say. In general, Mivart was more and suggested that in some cases they might happen to be interested in the fact that intermediate forms of traits did not well suited to their environment. For Goldschmidt, flat- seem to be useful. What good was half a wing to a bird, he fishes looked like promising candidates for hopeful wondered. What good was an eye that had not made it all monsters (Goldschmidt 1933). After all, he pointed out, the way around a flatfish’s head? no one had found a transition between ordinary fishes and Darwin took Mivart very seriously, and in 1872—the flatfishes. Perhaps, Goldschmidt suggested, it had only year after On the Genesis of Species came out—he took on taken a single mutation to launch a fish eye on its journey Mivart’s arguments in the sixth edition of the Origin of across the skull, and the basic flatfish anatomy emerged in Species. Mivart, Darwin argued, was not thinking carefully a flash. enough about what could or could not evolve by gradual In 2008, a graduate student at the University of Chicago evolution.