But in the eye of a fly the outputs of the six cells are not pooled with each other. Instead, each one is pooled with the outputs of particular cells from neighbouring ommatidia (Figure 5.27). In the interests of clarity, the scale is all wrong in this diagram. For the same reason, the arrows don't represent rays (which would be bent by the lenses) but mappings from points on the dolphin to points in the bottoms of tubes. Now, see the shattering ingenuity of this scheme. The essential idea is that those photocells that are looking at the head of the dolphin in one ommatidium are ganged together with those photocells that are looking at the head of the dolphin in neighbouring ommatidia. Those photocells that are looking at the tail of the dolphin in one ommatidium are wired up together with those photocells that are looking at the tail of the dolphin in neighbouring ommatidia. And so on. The result is that each bit of the dolphin is being signalled by a {188}
Figure 5.27 The ingenious principle of the ‘wired-up superposition compound eye.
larger number of photons than there would be in an ordinary apposition eye with a simple tube arrangement. It is a kind of computational, rather than an optical, solution to our old problem of how to augment the number of photons arriving from any one point on our dolphin. {189}
You can see why this is called superposition, even though it strictly isn't. In true superposition, using fancy lenses or mirrors, light coming through neighbouring facets is superimposed so that photons from the dolphin's head end up in the same place as other photons from the dolphin's head; photons from the tail end up in the same place as other photons from the tail. In neural superposition, the photons still end up in different places, as they would in an apposition eye. But the signal from those photons ends up in the same place, due to the artful plaiting of the wires leading to the brain.
Nilssons estimate for the rate of evolution of a camera eye was, you will recall, that it was by geological standards more or less instantaneous. You'd be lucky to find fossils that recorded the transitional stages. Exact estimates have not been done for compound eyes or any of the other designs of eye, but I doubt if they'd be significantly slower. One doesn't ordinarily expect to be able to see the details of eyes in fossils, because they are too soft to fossilize. Compound eyes are an exception because much of their detail is betrayed in the elegant array of more or less horny facets on the outer surface. Figure 5.28 shows a trilobite eye, from the Devonian era, nearly 400 million years ago. It looks just as advanced as a modern compound eye. This is what we should expect if the time it takes to evolve an eye is negligible by geological standards.
A central message of this chapter is that eyes evolve easily and fast, at the drop of a hat. I began by quoting the conclusion of one authority that eyes have evolved independently at least forty times in different parts of the animal kingdom. On the face of it, this message might seem challenged by an intriguing set of experimental results, recently reported by a group of workers in Switzerland associated with Professor Walter Gehring. I shall briefly explain what they found, and why it does not really challenge the conclusion of this chapter. Before I begin, I need to apologize for a maddeningly silly convention adopted by geneticists over the naming of genes. The gene called eyeless in the fruitfly Drosophila actually makes eyes! (Wonderful, isn't it?) The reason for this wantonly confusing piece of terminological contrariness is actually quite simple, and even rather interesting. We recognize what a gene does by noticing what happens when it goes {190}
Figure 5.28 Compound eyes were already very advanced 400 million years ago: fossilized trilobite eye.
wrong. There is a gene which, when it goes wrong (mutates), causes flies to have no eyes. The position on the chromosome of this gene is therefore named the eyeless locus (locus’ is the Latin for ‘place’ and it is used by geneticists to mean a slot on a chromosome where alternative forms of a gene sit). But usually when we speak of the locus named eyeless we are actually talking about the normal, undamaged form of the gene at that locus. Hence the paradox that the eyeless gene makes eyes. It is like calling a loudspeaker a ‘silence device’ because you have discovered that, when you take the loudspeaker out of a radio, the radio is silent. I shall have none of it. I am tempted to rename the gene eyemaker, but this would be confusing too. I shall certainly not call it eyeless and shall adopt the recognized abbreviation ey.
Now, it is a general fact that although all of an animal's genes are present in all its cells, only a minority of those genes are actually turned on or ‘expressed’ in any given part of the body. This is why {191} livers are different from kidneys, even though both contain the same complete set of genes. In the adult Drosophila, ey usually expresses itself only in the head, which is why the eyes develop there. George Haider, Patrick Callaerts and Walter Gehring discovered an experimental manipulation that led to ey's being expressed in other parts of the body. By doctoring Drosophila larvae in cunning ways, they succeeded in making ey express itself in the antennae, the wings and the legs. Amazingly, the treated adult flies grew up with fully formed compound eyes on their wings, legs, antennae and elsewhere (Figure 5.29), Though slightly smaller than ordinary eyes, these {192}
Figure 5.29 Induced ectopic eyes in Drosophilia; the bottom one has been induced by a mouse gene.
‘ectopic’ eyes are proper compound eyes with plenty of properly formed ommatidia. They even work. At least, we don't know that the flies actually see anything through them, but electrical recording from the nerves at the base of the ommatidia shows that they are sensitive to light.
That is remarkable fact number one. Fact number two is even more remarkable. There is a gene in mice called small eye and one in humans called aniridia. These, too, are named using the geneticists’ negative convention: mutational damage to these genes causes reduction or absence of eyes or parts of eyes. Rebecca Quiring and Uwe Waldorf, working in the same Swiss laboratory, found that {193}
these particular mammal genes are almost identical, in their DNA sequences, to the ey gene in Drosophila. This means that the same gene has come down from remote ancestors to modern animals as distant from each other as mammals and insects. Moreover, in both these major branches of the animal kingdom the gene seems to have a lot to do with eyes. Remarkable fact number three is almost too startling. Haider, Callaerts and Gehring succeeded in introducing the mouse gene into Drosophila embryos. Mirabile dictu, the mouse gene induced ectopic eyes in Drosophila. Figure 5.29 (bottom) shows a small compound eye induced on the leg of a fruitfly by the mouse equivalent of ey. Notice, by the way, that it is an insect compound eye that has been induced, not a mouse eye. The mouse gene has simply switched on the eyemaking developmental machinery of Drosophila. Genes with pretty much the same DNA sequence as ey have been found also in molluscs, marine worms called nemertines, and sea-squirts. Ey may very well be universal among animals, and it may turn out to be a general rule that a version of the gene taken from a donor in one part of the animal kingdom can induce eyes to develop in recipients in an exceedingly remote part of the animal kingdom.
What does this spectacular series of experiments mean for our conclusion in this chapter? Were we wrong to think that eyes have developed forty times independently? I don't think so. At least the spirit of the statement that eyes evolve easily and at the drop of a hat remains unscathed. These experiments probably do mean that the common ancestor of Drosophila, mice, humans, sea-squirts and so on had eyes. The remote common ancestor had vision of some kind, and its eyes, whatever form they may have taken, probably developed under the influence of a sequence of DNA similar to modern ey. But the actual form of the different kinds of eye, the details of retinas and lenses or mirrors, the choice of compound versus simple, and if compound the choice among apposition or various kinds of superposition, all these evolve independently and rapidly. We know this by looking at the sporadic — almost capricious — distribution of these various devices and systems, dotted around the animal kingdom. In {194} brief, animals often have an eye that resembles their remoter cousins more
than it resembles their closer cousins. The conclusion remains unshaken by the demonstration that the common ancestor of all these animals probably had eyes of some kind, and that the embryonic development of all eyes seems to have enough in common to be inducible by the same DNA sequence.
After Michael Land had kindly read and criticized the first draft of this chapter, I invited him to attempt a visual representation of the eye region of Mount Improbable and Figure 5.30 shows what he drew. It is in the nature of metaphors that they are good for some purposes but not others and we must be prepared to modify them, or even drop them altogether, when necessary. This is not the first occasion when the reader will have noticed that Mount Improbable, for all that it has a singular name like the Jungfrau, is actually a more complicated, multiple-peaked affair. {195}
Figure 5.30 The eye region of the Mount Improbable range: Michael Lands landscape of eye evolution.
That other great authority on animal eyes, Dan Nilsson, who also read the chapter in draft, summed up the central message by calling my attention to what may be the most bizarre example of the ad hoc and opportunistic evolution of an eye. Three times independently, in three different groups of fish, the so-called ‘four-eyed’ condition has evolved. Probably the most remarkable of the four-eyed fish is Bathylychnops exilis (Figure 5.31). It has a typical fish eye looking outwards in the usual direction. But a secondary eye has evolved in addition, lodged in the wall of the main eye and looking straight downwards. What it looks at, who knows? Perhaps Bathylychnops suffers from a terrible predator with the habit of approaching from below. From our point of view the interesting thing is this. The embryologi-cal development of the secondary eye is completely different from that of the main eye, although we may surmise that its development may turn out to be induced in nature by a version of the ey gene. In particular, as Dr Nilsson put it in his letter to me, ‘This species has re-invented the lens despite the fact it already had one. It serves as a good support for the view that lenses are not difficult to evolve.’
Nothing is as difficult to evolve as we humans imagine it to be. Darwin gave too much when he bent over backwards to concede the difficulty of evolving an eye. And his wife took too much when she underlined her scepticism in the margin. Darwin knew what he was {196}
Figure 5.31 A remarkable double eye, that of the fish Bathylychnops exilis.
doing. Creationists love the quotation that I gave at the beginning of this chapter, but they never complete it. After making his rhetorical concession, Darwin went on:
When it was first said that the sun stood still and the world turned round, the common sense of mankind declared the doctrine false; but the old saying of Vox populi, vox Dei, as every philosopher knows, cannot be trusted in science. Reason tells me, that if numerous gradations from an imperfect and simple eye to one perfect and complex, each grade being useful to its possessor, can be shown to exist, as is certainly the case; if further, the eye ever slightly varies, and the variations be inherited, as is likewise certainly the case; and if such variations should ever be useful to any animal under changing conditions of life, then the difficulty of believing that a perfect and complex eye could be formed by natural selection, though insuperable by our imagination, cannot be considered real. {197}
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CHAPTER 6
NATURAL SELECTION IS THE PRESSURE THAT DRIVES evolution up the slopes of Mount Improbable. Pressure really is rather a good metaphor. We speak of ‘selection pressure’, and you can almost feel it pushing a species to evolve, shoving it up the gradients of the mountain. Predators, we say, provided the selection pressure that drove antelopes to evolve their fast running legs. Even as we speak, though, we remember what this really means: genes for short legs are more likely to end up in predators’ bellies and therefore the world becomes less full of them. ‘Pressure’ from choosy females drove the evolution of male pheasants’ sumptuous feathers. What this means is that a gene for a beautiful feather is especially likely to find itself riding a sperm into a female's body. But we think of it as a ‘pressure’ driving males towards greater beauty. No doubt predators provided a selection pressure in the opposite direction, towards duller plumage, since bright males would presumably attract predator, as well as female, eyes. Without the pressure from predators the cocks would be even brighter and more extravagant under pressure from females. Selection pressures, then, can push in opposite directions, or in the same direction or even (mathematicians can find ways of visualizing this) at any other ‘angle’ relative to one another. Selection pressures, moreover, can be ‘strong’ or ‘weak’, and the ordinary-language meanings of these words fit well. The particular path up {198} Mount Improbable that a lineage takes will be influenced by lots of different selection pressures, pushing and tugging in different directions and with different strengths, sometimes cooperating with each other, sometimes opposing.
But pressure isn't the end of the story. The path chosen up Mount Improbable will depend, too, on the shapes of the slopes. There are selection pressures, pushing and tugging in an assortment of directions and strengths, but there are also lines of least resistance and insurmountable precipices. A selection pressure may push for all it's worth in a particular direction, but if that direction is blocked by an impassable cliff it will come to nothing. Natural selection has to have alternatives to choose among. Selection pressures, however strong, can't do anything without genetic variation. To say that predators provide a selection pressure in favour of fast-running antelopes is just to say that predators eat the slowest antelopes. But if there is nothing to choose between the genes of fast and slow antelopes — that is, if differences in running speed are purely environmentally determined — no evolutionary business will result. In the direction of improved speed, Mount Improbable might present no slope to climb.
Now we come to a piece of genuine uncertainty and a spectrum of opinion among biologists. At one extreme are those who feel that we can take genetic variation more or less for granted. If the selection pressure exists, they feel, there will always be enough genetic variation to accommodate it. The trajectory of a lineage in evolutionary space will be, in practice, determined by the tussle among selection pressures alone. At the other extreme are those who feel that available genetic variation is the important consideration determining the direction of evolution. Some even go so far as to assign natural selection a minor, subsidiary role. To take our two biologists to the point of caricature, we might imagine them disagreeing on why pigs don't have wings. The extreme selectionist says that pigs don't have wings because it would not be an advantage for them to have wings. The extreme anti-selectionist says that pigs might benefit from having wings, but they can't have them because there never were mutant wing stubs for natural selection to work upon. {199}
The controversy is more sophisticated than that, and Mount Improbable, even in its multiple-peaked version, isn't a powerful enough metaphor to explore it. We need a new metaphor, using the kind of imagination that mathematicians enjoy although we shan't use explicit mathematical symbols. It will make more demands on us than Mount Improbable, but it is worth it. In The Blind Watchmaker I made brief excursions into what I variously called ‘genetic space’, ‘biomorph land’ and ‘Making Tracks Through Animal Space’. More recently the philosopher Daniel Dennett has penetrated further into this undiscovered country which, by poetic allusion to Borges s Library of Babel, he calls the Library of Mendel. My version in this chapter is a gigantic museum of the zoological imagination.
Imagine a museum with galleries stretching towards the horizon in every direction, and as far as the eye can see upwards and downwards as well. Preserved in the museum is every kind of animal form that has ever existed, and every kind that could be imagined. Each animal is housed next door to those that it most resembles. Each dimension in the museum — that is, each direction along which a gallery extends — corresponds to one dimension in which die animals vary. For example, as you walk north a
long a particular gallery you notice a progressive lengthening of die horns of the specimens in die cabinets. Turn round and walk south and the horns shorten. Turn and walk east and the horns stay the same but something else changes, say the teeth get sharper. Walk west and the teeth grow blunter. Since horn length and tooth sharpness are only two out of thousands of ways in which animals can vary, the galleries must criss-cross one another in many-dimensional space, not just the ordinary three-dimensional space that we, with our limited minds, are capable of visualizing. This is what I meant when I said that we had to learn to think like a mathematician.
What would it mean to think in four dimensions? Suppose we are dealing with antelopes and we measure four variables: horn length, tooth sharpness, intestine length and coat hairiness. If we ignore one of the dimensions, say coat hairiness, we could place each of our antelopes in its rightful place in a three-dimensional graph — a cube — of die remaining variables, horn length, tooth sharpness and intestine length. Now how do we bring in the fourth dimension, coat hairiness? We do {200} the whole cube exercise separately for all short-haired antelopes, then we produce another cube for all slightly longer-haired antelopes and so on. A given antelope will be placed, first in whichever cube pertains to its hair length and then, within that cube, to its rightful position determined by its horns, teeth and intestines. Coat hairiness is the fourth dimension. In principle you can go on constructing families of cubes, and cubes of cubes, and cubes of cubes of cubes until you have placed animals in the equivalent of many-dimensional space.