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Old World monkeys join. This phylogeny of the 100 or so species of Old World monkey is generally accepted. The circles now visible at the tips of the branches indicate the number of known species in each group as an order of magnitude: no circle means 19 known species, a small width circle means 1099, a larger circle, 100999, etc.; each of the four groups shown contain between 10 and 99 species. This phylogeny of the 100 or so species of Old World monkey is generally accepted. The circles now visible at the tips of the branches indicate the number of known species in each group as an order of magnitude: no circle means 19 known species, a small width circle means 1099, a larger circle, 100999, etc.; each of the four groups shown contain between 10 and 99 species.

Images, left to right: mandrill ( mandrill (Mandrillus sphinx); redtail monkey (Cercopithecus ascanius); proboscis monkey (Nasalis larvatus); Angolan black-and-white colobus (Colobus angolensis).

What, then, should we call the intermediates between Concestor 5 and Proconsul Proconsul before they lost their tail? A strict cladist would call them apes, because they lie on the ape side of the fork. A different kind of taxonomist would call them monkeys because they were tailed. Not for the first time, I say it is silly to become too worked up over names. before they lost their tail? A strict cladist would call them apes, because they lie on the ape side of the fork. A different kind of taxonomist would call them monkeys because they were tailed. Not for the first time, I say it is silly to become too worked up over names.

The Old World monkeys, Cercopithecidae, are a true clade, a group that includes all descendants of a single common ancestor. However 'monkeys' as a whole are not, because they include the New World monkeys, Platyrrhini. The Old World monkeys are closer cousins to apes, with whom they are united in the Catarrhini, than to New World monkeys. All apes and monkeys together const.i.tute a natural clade, the Anthropoidea. 'Monkeys' const.i.tutes an artificial (technically 'paraphyletic') grouping because it includes all the platyrrhines plus some of the catarrhines but excluding the ape portion of the catarrhines. It might be better to call the Old World monkeys tailed apes. Catarrhine, as I mentioned earlier, means 'down nose': the nostrils face downwards in this respect we are ideal catarrhines. Voltaire's Dr Pangloss observed that 'the nose is formed for spectacles, therefore we come to wear spectacles'. He could have added that our catarrhine nostrils are beautifully directed to keep out the rain. Platyrrhine means flat or broad nose. It is not the only diagnostic difference between these two great groups of primates, but it is the one that gives them their names. Let's press on to Rendezvous 6 Rendezvous 6, and meet the platyrrhines.

Rendezvous 6.

NEW WORLD MONKEYS.

Rendezvous 6, where the New World platyrrhine 'monkeys' meet us and our approximately 3-million-greats-grandparent, Concestor 6, the first anthropoid, is some 40 million years ago. It was a time of lush tropical forests even Antarctica was at least partly green in those days. Although all platyrrhine monkeys now live in South or Central America, the rendezvous itself almost certainly did not take place there. My guess is that Rendezvous 6 Rendezvous 6 is somewhere in Africa. A group of African primates with flat noses, who have left no surviving African descendants, somehow managed, in the form of a small founding population, to get across to South America. We don't know when this happened, but it was before 25 million years ago (when the first monkey fossils appear in South America) and after 40 million years ago ( is somewhere in Africa. A group of African primates with flat noses, who have left no surviving African descendants, somehow managed, in the form of a small founding population, to get across to South America. We don't know when this happened, but it was before 25 million years ago (when the first monkey fossils appear in South America) and after 40 million years ago (Rendezvous 6). South America and Africa were closer to each other than they are now, and sea levels were low, perhaps exposing a chain of islands across the gap from West Africa, convenient for island-hopping. The monkeys probably rafted across, perhaps on fragments of mangrove swamps that could support life as floating islands for a short while. Currents were in the right direction for inadvertent rafting. Another major group of animals, the hystricognath rodents, probably arrived in South America around the same time. Again probably they came from Africa, and indeed they are named after the African porcupine, Hystrix Hystrix. Probably the monkeys rafted across the same island chain as the rodents, using the same favourable currents, though presumably not the same rafts.

Are all the New World primates descended from a single immigrant? Or was the island-hopping corridor used1 more than once by primates? What would const.i.tute positive evidence for a double immigration? In the case of the rodents, there are still hystricognath rodents in Africa, including African porcupines, mole rats, da.s.sie rats and cane rats. If it turned out that some of the South American rodents were close cousins of some African ones (say porcupines) while other South American rodents were closer cousins to other African ones (say mole rats) this would be good evidence that rodents more than once drifted to South America. That this is not the case is compatible with the view that rodents dispersed to South America only once, though it is not strong evidence. The South American primates, too, are all closer cousins to each other than they are to any African primate. Again this is compatible with the hypothesis of a single dispersal event, but again the evidence is not strong. more than once by primates? What would const.i.tute positive evidence for a double immigration? In the case of the rodents, there are still hystricognath rodents in Africa, including African porcupines, mole rats, da.s.sie rats and cane rats. If it turned out that some of the South American rodents were close cousins of some African ones (say porcupines) while other South American rodents were closer cousins to other African ones (say mole rats) this would be good evidence that rodents more than once drifted to South America. That this is not the case is compatible with the view that rodents dispersed to South America only once, though it is not strong evidence. The South American primates, too, are all closer cousins to each other than they are to any African primate. Again this is compatible with the hypothesis of a single dispersal event, but again the evidence is not strong.

This is a good moment to repeat that the improbability of a rafting event is very far from being a reason for doubting that it happened. This sounds surprising. Usually, in everyday life, ma.s.sive improbability is a good reason for thinking that something won't happen. The point about intercontinental rafting of monkeys, or rodents or anything else, is that it only had to happen once, and the time available for it to happen, in order to have momentous consequences, is way outside what we can grasp intuitively. The odds against a floating mangrove bearing a pregnant female monkey and reaching landfall in any one year may be ten thousand to one against. That sounds tantamount to impossible by the lights of human experience. But given 10 million years it becomes almost inevitable. Once it happened, the rest was easy. The lucky female gave birth to a family, which eventually became a dynasty, which eventually branched to become all the species of New World monkeys. It only had to happen once: great things then grew from small beginnings.

In any case, accidental rafting is not nearly so rare as you might think. Small animals are often seen on flotsam. And the animals aren't always small. The green iguana is typically a metre long and can be up to two metres. I quote from a note to Nature Nature by Ellen J. Censky and others: by Ellen J. Censky and others: On 4 October 1995, at least 15 individuals of the green iguana, Iguana iguana Iguana iguana, appeared on the eastern beaches of Anguilla in the Caribbean.

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New World monkeys join. The phylogeny of the 100 or so species of New World monkeys is somewhat disputed, but here we follow the modern consensus. The phylogeny of the 100 or so species of New World monkeys is somewhat disputed, but here we follow the modern consensus.

Images, left to right: golden lion tamarin ( golden lion tamarin (Leontopithecus rosalia); owl monkey (Aotus trivirgatus); squirrel monkey (Saimiri sciureus); black howler monkey (Alouatta caraya); monk saki (Pithecia monachus).

This species did not previously occur on the island. They arrived on a mat of logs and uprooted trees, some of which were more than 30 feet long and had large root ma.s.ses. Local fishermen say the mat was extensive and took two days to pile up on sh.o.r.e. They reported seeing iguanas on both the beach and on logs in the bay.

The iguanas were presumably roosting in trees on some other island, which were uprooted and sent to sea by a hurricane: either Luis, which had raged through the Eastern Caribbean on 45 September, or Marilyn, a fortnight later. Neither hurricane hit Anguilla. Censky and her colleagues subsequently caught or sighted green iguanas on Anguilla, and on an islet half a kilometre off sh.o.r.e. The population still survived on Anguilla in 1998 and included at least one reproductively active female. Iguanas and related lizards, by the way, are especially good at colonising islands, all over the world. Iguanas even occur on Fiji and Tonga, which are much more remote than the West Indian islands.

I can't resist remarking how chilling this kind of 'it only had to happen once' logic becomes when you apply it to contingencies nearer home. The principle of nuclear deterrence, and the only remotely defensible justification for possessing nuclear weapons, is that n.o.body will dare risk a first strike, for fear of ma.s.sive retaliation. What are the odds against a mistaken missile launch: a dictator who goes mad; a computer system that malfunctions; an escalation of threats that gets out of hand? What are the odds against a terrible mistake, initiating Armageddon? A hundred to one against, within any one year? I would be more pessimistic. We came awfully close in 1963. What might happen in Kashmir? Israel? Korea? Even if the odds per year are as low as one in a hundred, a century is a very short time, given the scale of the disaster we are talking about. It only has to happen once.

Let's return to a happier topic, the New World monkeys. As well as walking quadrupedally above branches, like many Old World monkeys, some New World monkeys suspend themselves like gibbons, and even brachiate. The tail is prominent in all the New World monkeys, and in the spider monkeys, woolly monkeys and howler monkeys it is prehensile, wielded like an extra arm. They can happily hang from the tail alone, or from any combination of arms, legs and tail. The tail doesn't have a hand at the end, but you almost believe it has, when you watch a spider monkey.2 New World monkeys also include some spectacularly acrobatic leapers, as well as the only nocturnal anthropoids, the owl monkeys. Like owls and cats, owl monkeys have large eyes the largest eyes of all the monkeys or apes. Pygmy marmosets are the size of a dormouse, smaller than any other anthropoid. The largest howler monkeys, however, are only about as big as a large gibbon. Howlers resemble gibbons, too, in being good at hanging and swinging from their arms, and in being very noisy but where gibbons sound like New York police sirens in full cry, a troop of howler monkeys, with their resonating hollow bony voice boxes, remind me more of a ghost squadron of jet planes, roaring eerily through the treetops. As it happens, howler monkeys have a particular tale to tell us Old World monkeys about the way we see colour, for they have independently arrived at the same solution.

THE HOWLER MONKEY'S TALE.

Written with Yan Wong.

New genes aren't added to the genome out of thin air. They originate as duplicates of older genes. Then, over evolutionary time, they go their separate ways by mutation, selection and drift. We don't usually see this happening but, like detectives arriving on the scene after a crime, we can piece together what must have happened from the evidence that remains. The genes involved in colour vision provide a striking example. For reasons that will emerge, the howler monkey is especially well placed to tell the tale.

During their formative megayears, mammals were creatures of the night. The day belonged to the dinosaurs, who probably, if their modern relatives are any guide, had superb colour vision. So, we may plausibly imagine, did the mammals' remote ancestors, the mammal-like reptiles, who filled the days before the rise of the dinosaurs. But during the mammals' long nocturnal exile, their eyes needed to snap up whatever photons were available, regardless of colour. Not surprisingly, for reasons of the kind that we shall examine in the Blind Cave Fish's Tale, colour discrimination degenerated. To this day most mammals, even those who have returned to live in the daylight, have rather poor colour vision, with only a two-colour system ('dichromatic'). This refers to the number of different cla.s.ses of colour-sensitive cells 'cones' in the retina. We catarrhine apes and Old World monkeys have three: red, green and blue, and are therefore trichromatic, but the evidence suggests that we regained regained a third cla.s.s of cone, after our nocturnal ancestors lost it. Most other vertebrates, such as fish and reptiles but a third cla.s.s of cone, after our nocturnal ancestors lost it. Most other vertebrates, such as fish and reptiles but not not mammals, have three-cone ('trichromatic') or four-cone ('tetrachromatic') vision, and birds and turtles can be even more sophisticated. We'll come to the very special situation in the New World monkeys, and the even more special situation in the howler monkey, in a moment. mammals, have three-cone ('trichromatic') or four-cone ('tetrachromatic') vision, and birds and turtles can be even more sophisticated. We'll come to the very special situation in the New World monkeys, and the even more special situation in the howler monkey, in a moment.

Interestingly, there is evidence that Australian marsupials differ from most mammals in having good trichromatic colour vision. Catherine Arrese and her colleagues, who discovered this in honey possums and dunnarts (it has also been demonstrated in wallabies), suggest that Australian (but not American) marsupials kept an ancestral reptilian visual pigment that the rest of the mammals lost. But mammals in general probably have the poorest colour vision among vertebrates. Most mammals see colour, if at all, only as well as a colourblind man. The notable exceptions are to be found among primates, and it is no accident that they, more than any other group of mammals, make use of bright colours in s.e.xual display.

Unlike the Australian marsupials who perhaps never lost it, we can tell by looking at our relatives among the mammals that we primates did not retain trichromatic vision from our reptilian ancestors but rediscovered it not once, but twice independently: first in the Old World monkeys and apes; and second in the New World howler monkeys, although not among the New World monkeys generally. Howler monkey colour vision is like that of apes, but different enough to betray its independent origin.

Why would good colour vision be so important that trichromacy evolved independently in New and Old World monkeys? A favoured suggestion is that it has to do with eating fruit. In a predominantly green forest, fruits stand out by their colours. This, in turn, is no accident. Fruits have probably evolved bright colours to attract frugivores, such as monkeys, who play the vital role of spreading and manuring their seeds. Trichromatic vision also a.s.sists in the detection of younger, more succulent leaves (often pale green, sometimes even red), against a background of darker green but that is presumably not to the advantage of the plants.

Colour dazzles our awareness. Colour words are among the first adjectives that infants learn, and the ones they most eagerly tie to any noun that's going. It is hard to remember that the hues we perceive are labels for electromagnetic radiations of only slightly differing wavelengths. Red light has a wavelength around 700 billionths of a metre, violet around 420 billionths of a metre, but the whole gamut of visible electromagnetic radiation that lies between these bounds is an almost ludicrously narrow window, a tiny fraction of the total spectrum whose wavelengths range from kilometres (some radio waves) down to fractions of a nanometre (gamma rays).

All eyes on our planet are set up in such a way as to exploit the wavelengths of electromagnetic radiation in which our local star shines brightest, and which pa.s.s through the window of our atmosphere. For an eye that has committed itself to biochemical techniques suitable for this loosely bounded range of wavelengths, the laws of physics impose sharper bounds to the portion of the electromagnetic spectrum that can be seen using those techniques. No animal can see far into the infrared. Those that come closest are pit vipers, who have pits in the head which, while in no sense focusing a proper image with infrared rays, allow these snakes to achieve some directional sensitivity to the heat generated by their prey. And no animal can see far into the ultraviolet although some, bees for instance, can see a bit further than we can. But on the other hand, bees can't see our red: for them it is infrared. All animals agree that 'light' is a narrow band of electromagnetic wavelengths lying somewhere between ultraviolet at the short end and infrared at the long end. Bees, people and snakes differ only slightly in where they draw the lines at each end of 'light'.

An even narrower view is taken by each of the different kinds of light-sensitive cells within a retina. Some cones are slightly more sensitive towards the red end of the spectrum, others towards the blue. It is the comparison between cones that makes colour vision possible, and the quality of colour vision depends largely on how many different cla.s.ses of cones there are to compare. Dichromatic animals have only two populations of cones interspersed with one another. Trichromats have three, tetrachromats four. Each cone has a graph of sensitivity, which peaks somewhere in the spectrum and fades away, not particularly symmetrically, on either side of the peak. Out beyond the edges of its sensitivity graph, the cell may be said to be blind.

Suppose a cone's sensitivity peaks in the green part of the spectrum. Does this mean, if that cell is firing impulses towards the brain, that it is looking at a green object like gra.s.s or a billiard table? Emphatically not. It is just that the cell would need more red light (say) to achieve the same firing rate as a given amount of green light. Such a cell would behave identically towards bright red light or dimmer green light.3 The nervous system can tell the colour of an object only by The nervous system can tell the colour of an object only by comparing comparing the simultaneous firing rates of (at least) two cells that favour different colours. Each one serves as a 'control' for the other. You can get an even better idea of the colour of an object by comparing the firing rate of three cells, all with different sensitivity graphs. the simultaneous firing rates of (at least) two cells that favour different colours. Each one serves as a 'control' for the other. You can get an even better idea of the colour of an object by comparing the firing rate of three cells, all with different sensitivity graphs.

Colour television and computer screens, doubtless because they are designed for our trichromatic eyes, also work on a three-colour system. On a normal computer monitor, each 'pixel' consists of three dots placed too close together for the eye to resolve. Each dot always glows with the same colour if you look at the screen at sufficient magnification you always see only the same three colours, usually red, green and blue although other combinations can do the job. Flesh tones, subtle shades any hue you wish can be achieved by manipulating the intensities with which these three primary colours glow. Tetrachromatic turtles, for example, might be disappointed by the unrealistic (to them) pictures on our television and cinema screens.

By comparing the firing rates from just three kinds of cones, our brains can perceive a huge range of hues. But most placental mammals, as already stated, are not trichromats but dichromats, with only two populations of cones in their retinas. One cla.s.s peaks in the violet (or in some cases the ultraviolet), the other cla.s.s peaks somewhere between green and red. In us trichromats, the short wavelength cones peak between violet and blue, and they are normally called blue cones. Our other two cla.s.ses of cones can be called green cones and red cones. Confusingly, even the 'red' cones peak at a wavelength that is actually yellowish. But their sensitivity curve as a whole stretches into the red end of the spectrum. Even if they peak in the yellow, they still fire strongly in response to red light. This means that, if you subtract the firing rate of a 'green' cone from that of a 'red' cone, you'll get an especially high result when looking at red light. From now on I shall forget about peak sensitivities (violet, green and yellow) and refer to the three cla.s.ses of cones as blue, green and red. In addition to cones, there are also rods: light-sensitive cells of a different shape from cones, which are especially useful at night and which are not used in colour vision at all. They'll play no further part in our story.

The chemistry and the genetics of colour vision are rather well understood. The main molecular actors in the story are opsins: protein molecules which serve as visual pigments sitting in the cones (and rods). Each opsin molecule works by attaching to, and encasing, a single molecule of retinal: a chemical derived from vitamin A.4 The retinal molecule has been forcibly kinked beforehand to fit it into the opsin. When hit by a single photon of light of an appropriate colour, the kink straightens out. This is the signal to the cell to fire a nervous impulse, which says to the brain 'my kind of light The retinal molecule has been forcibly kinked beforehand to fit it into the opsin. When hit by a single photon of light of an appropriate colour, the kink straightens out. This is the signal to the cell to fire a nervous impulse, which says to the brain 'my kind of light here here'. The opsin molecule is then recharged with another kinked retinal molecule, from a store in the cell.

Now, the important point is that not all opsin molecules are the same. Opsins, like all proteins, are made under the influence of genes. DNA differences result in opsins that are sensitive to light of different wavelengths, and this is the genetic basis of the two-colour or three-colour systems we have been talking about. Of course, since all genes are present in all cells, the difference between a red cone and a blue cone is not which genes they possess, but which genes they turn on. And there is some kind of rule that says that any one cone only only turns on one cla.s.s of gene. turns on one cla.s.s of gene.

The genes that make our green and red opsins are very similar to each other, and they are on the X chromosome (the s.e.x chromosome of which females have two copies and males only one). The gene that makes the blue opsin is a bit different, and lies not on a s.e.x chromosome but on one of the ordinary non-s.e.x chromosomes called autosomes (in our case it is chromosome 7). Our green and red cells have clearly been derived from a recent gene duplication event, and much longer ago they must have diverged from the blue opsin gene in another duplication event. Whether an individual has dichromatic or trichromatic vision depends on how many distinct opsin genes it has in its genome. If it has, say, blue- and green-sensitive opsins but not red, it will be a dichromat.

That's the background to how colour vision works in general. Now, before we come to the special case of the howler monkey itself and how it became trichromatic, we need to understand the strange dichromatic system of the rest of the New World monkeys (some lemurs have it too, by the way, and not all New World monkeys do for example, nocturnal owl monkeys have monochromatic vision). For the purposes of this discussion, 'New World monkey' temporarily excludes howler monkeys and other exceptional species. We'll come to the howler monkeys later.

First, set aside the blue gene as an unvarying fixture on an autosome, present in all individuals whether male or female. The red and green genes, on the X chromosome, are more complicated and will occupy our attention. Each X chromosome has only one locus where a red or a green5 allele might sit. Since a female has two X chromosomes, she has two opportunities for a red or green gene. But a male, with only one X chromosome, has allele might sit. Since a female has two X chromosomes, she has two opportunities for a red or green gene. But a male, with only one X chromosome, has either either a red or a green gene but a red or a green gene but not not both. So a typical male New World monkey has to be dichromatic. He has only two kinds of cones: blue plus both. So a typical male New World monkey has to be dichromatic. He has only two kinds of cones: blue plus either either red or green. By our standards, all males are colourblind, but they are colourblind in two different ways; some males within a population lack green opsins, others lack red opsins. All have blue. red or green. By our standards, all males are colourblind, but they are colourblind in two different ways; some males within a population lack green opsins, others lack red opsins. All have blue.

Females are potentially more fortunate. Having two X chromosomes, they could be lucky enough to have a red gene on one and a green gene on the other (plus the blue which again goes without saying). Such a female would be a trichromat.6 But an unlucky female might have two reds, or two greens, and would therefore be a dichromat. By our standards such females are colourblind, and in two ways, just like males. But an unlucky female might have two reds, or two greens, and would therefore be a dichromat. By our standards such females are colourblind, and in two ways, just like males.

A population of New World monkeys such as tamarins or squirrel monkeys, therefore, is an oddly complicated mixture. All males, and some females, are dichromats: colourblind by our standards but in two alternative ways. Some females, but no males, are trichromats, with true colour vision which is presumably similar to ours. Experimental evidence with tamarins searching for food in camouflaged boxes showed that trichromatic individuals were more successful than dichromats. Perhaps foraging bands of New World monkeys rely on their lucky trichromat females to find food that most of them would otherwise miss. On the other hand, there is a possibility that the dichromats, either alone or in collusion with dichromats of the other kind, might have strange advantages. There are anecdotes of bomber crews in the Second World War deliberately recruiting one colourblind member because he could spot certain types of camouflage better than his otherwise more fortunate trichromat comrades. Experimental evidence confirms that human dichromats can indeed break certain forms of camouflage that fool trichromats. Is it possible that a troop of monkeys consisting of trichromats and two kinds of dichromats might collectively find a greater variety of fruits than a troop of pure trichromats? This might sound far-fetched, but it is not silly.

The red and the green opsin genes in New World monkeys const.i.tute an example of a 'polymorphism'. Polymorphism is the simultaneous existence, in a population, of two or more alternative versions of a gene, where neither is rare enough to be just a recent mutant. It is a well-established principle of evolutionary genetics that visible polymorphisms like this don't just happen without good reason. Unless something very special is going on, monkeys with the red gene will be either better off, or worse off, than monkeys with the green gene. We don't know which, but it is highly unlikely that they would be exactly equally good. And the inferior kind should go extinct.

A stable polymorphism in a population, then, indicates that something special is going on. What sort of thing? Two main suggestions have been made for polymorphisms in general, and either might apply to this case: frequency-dependent selection, and heterozygous advantage. Frequency-dependent selection happens when the rarer type is at an advantage, simply by virtue of being rarer. So, as the type which we had thought was 'inferior' starts to go extinct, it ceases to be inferior and bounces back. How could this be? Well, suppose 'red' monkeys are especially good at seeing red fruits while 'green' monkeys are especially good at seeing green fruits. In a population dominated by red monkeys, most of the red fruits will be already taken, and a lone green monkey, able to see green fruits, might be at an advantage and vice versa. Even if that is not especially plausible, it is an example of the kind kind of special circ.u.mstance that can maintain both types in a population, without one of them going extinct. It is not hard to see that something along the lines of our 'bomber crew' theory might be the kind of special circ.u.mstance that maintains a polymorphism. of special circ.u.mstance that can maintain both types in a population, without one of them going extinct. It is not hard to see that something along the lines of our 'bomber crew' theory might be the kind of special circ.u.mstance that maintains a polymorphism.

Turning now to heterozygous advantage, the cla.s.sic example cliche almost is sickle-cell anaemia in humans. The sickling gene is bad, in that individuals with two copies of it (h.o.m.ozygotes) have damaged blood corpuscles that look like sickles, and suffer from debilitating anaemia. But it is good in that individuals with only one copy (heterozygotes) are protected against malaria. In areas where malaria is a problem, the good outweighs the bad, and the sickling gene tends to spread through the population, in spite of the adverse effects on individuals unlucky enough to be h.o.m.ozygotes.7 Professor John Mollon and his colleagues, whose research is mainly responsible for uncovering the polymorphic system of colour vision in New World monkeys, propose that the heterozygous advantage enjoyed by the trichromatic females is enough to favour the coexistence of the red and green genes in the population. But the howler monkey does it better, and this brings us to the teller of the tale itself. Professor John Mollon and his colleagues, whose research is mainly responsible for uncovering the polymorphic system of colour vision in New World monkeys, propose that the heterozygous advantage enjoyed by the trichromatic females is enough to favour the coexistence of the red and green genes in the population. But the howler monkey does it better, and this brings us to the teller of the tale itself.

Howler monkeys have managed to enjoy the virtues of both sides of the polymorphism, by combining them in one chromosome. They have done this by means of a lucky translocation. Translocation is a special kind of mutation. A chunk of chromosome somehow gets pasted into a different chromosome by mistake, or into a different place on the same chromosome. This seems to have happened to a lucky mutant ancestor of the howler monkeys, which consequently ended up with both both a red gene and a green gene next door to one another on a single X chromosome. This monkey would have been well on its evolutionary way towards becoming a true trichromat, even if it was a male. The mutant X chromosome spread through the population until, now, all howler monkeys have it. a red gene and a green gene next door to one another on a single X chromosome. This monkey would have been well on its evolutionary way towards becoming a true trichromat, even if it was a male. The mutant X chromosome spread through the population until, now, all howler monkeys have it.

It was easy for howler monkeys to perform this evolutionary trick, because the three opsin genes were already knocking around the population in New World monkeys: it is just that, with the exception of a few lucky females, any one individual monkey had only two of them. When we apes and Old World monkeys independently did the same kind of thing, we did it differently. The dichromats from which we sprang were dichromats in only one way: there wasn't a polymorphism to take off from. Evidence suggests that the doubling up of the opsin gene on the X chromosome in our ancestry was a true duplication. The original mutant found itself with two tandem copies of an identical gene, say two greens next door to each other on the chromosome, and it therefore was not a near-instant trichromat like the ancestral howler monkey mutant. It was a dichromat, with a blue and two green genes. The Old World monkeys became trichromats gradually in subsequent evolution, as natural selection favoured a divergence of the colour sensitivities of the two X opsin genes, towards green and red respectively.

When a translocation happens, it isn't just the gene of interest that is seen to move. Sometimes its travelling companions its neighbours on the original chromosome who move with it to the new chromosome can tell us something. And so it is in this case. The gene called Alu Alu is well known as a 'transposable element': a short, virus-like piece of DNA that replicates itself around the genome, as a sort of parasite, by subverting the cell's DNA replication machinery. Was is well known as a 'transposable element': a short, virus-like piece of DNA that replicates itself around the genome, as a sort of parasite, by subverting the cell's DNA replication machinery. Was Alu Alu responsible for moving the opsin? It seems so. We find the 'smoking gun' when we look at the details. There are responsible for moving the opsin? It seems so. We find the 'smoking gun' when we look at the details. There are Alu Alu genes at both ends of the duplicated region. Probably the duplication was an unintended by-product of parasitic reproduction. In some long-forgotten monkey of the Eocene Epoch, a genomic parasite near to the opsin gene tried to reproduce, accidentally replicated a much larger chunk of DNA than intended, and set us on the road to three-colour vision. Beware, by the way, of the temptation it is all too common to think that, because a genomic parasite seems, with hindsight, to have done us a favour, genomes therefore harbour parasites in the hope of future favours. That isn't how natural selection works. genes at both ends of the duplicated region. Probably the duplication was an unintended by-product of parasitic reproduction. In some long-forgotten monkey of the Eocene Epoch, a genomic parasite near to the opsin gene tried to reproduce, accidentally replicated a much larger chunk of DNA than intended, and set us on the road to three-colour vision. Beware, by the way, of the temptation it is all too common to think that, because a genomic parasite seems, with hindsight, to have done us a favour, genomes therefore harbour parasites in the hope of future favours. That isn't how natural selection works.

Whether engineered by Alu Alu or not, mistakes of this kind still sometimes happen. When two X chromosomes line up, prior to crossing over, it is possible for them to line up incorrectly. Instead of lining the red gene on one chromosome with the corresponding red on the other, the similarity of the genes can confuse the lining-up process so that a red is lined up with a green. If crossing over then happens it is 'unequal': one chromosome could end up with an extra green (say) while the other X chromosome gets no green gene at all. Even if crossing over doesn't happen, a process called 'gene conversion' can take place, where a short sequence of one chromosome is converted to the matching sequence in the other. With misaligned chromosomes, a part of the red gene may be replaced by the equivalent part of the green gene, or vice versa. Both unequal crossing over and misaligned gene conversion can lead to redgreen colourblindness. or not, mistakes of this kind still sometimes happen. When two X chromosomes line up, prior to crossing over, it is possible for them to line up incorrectly. Instead of lining the red gene on one chromosome with the corresponding red on the other, the similarity of the genes can confuse the lining-up process so that a red is lined up with a green. If crossing over then happens it is 'unequal': one chromosome could end up with an extra green (say) while the other X chromosome gets no green gene at all. Even if crossing over doesn't happen, a process called 'gene conversion' can take place, where a short sequence of one chromosome is converted to the matching sequence in the other. With misaligned chromosomes, a part of the red gene may be replaced by the equivalent part of the green gene, or vice versa. Both unequal crossing over and misaligned gene conversion can lead to redgreen colourblindness.

Men suffer more frequently from redgreen colourblindness than women (the suffering is not great, but it is still a nuisance and they presumably are deprived of aesthetic experiences enjoyed by the rest of us) because if they inherit one faulty X chromosome they do not have another to serve as a backup. n.o.body knows whether they see blood and gra.s.s in the way the rest of us see blood, or in the way the rest of us see gra.s.s, or whether they see both in some completely different way. Indeed, it may vary from person to person. All we know is that people who are redgreen colourblind think gra.s.s-like things are pretty much the same colour as blood-like things. In humans, dichromatic colourblindness afflicts about two per cent of males. Don't be confused, incidentally, by the fact that other kinds of redgreen colourblindness are more common (affecting about eight per cent of males). These individuals are called anomalous trichromats: genetically they are trichromats, but one of their three kinds of opsins doesn't work.8 Unequal crossing over doesn't always make things worse. Some X chromosomes end up with more than two opsin genes. The extra ones nearly always seem to be green rather than red. The record number is a staggering twelve extra green genes, arrayed in tandem. But there is no evidence that individuals with extra green genes can see any better. Nevertheless, the high mutation rate along this part of the X chromosome means that not all 'green' genes in the population are exactly the same as each other. So it is theoretically possible for a female, with her two X chromosomes, to have not trichromatic vision but vision which is tetrachromatic (or even pentachromatic, if her red genes also differ). I don't know that anybody has tested this.

It is possible that an uneasy thought has occurred to you. I have talked as though the acquisition, by mutation, of a new opsin automatically confers enhanced colour vision. But of course differences between the colour sensitivities of cones are no earthly use unless the brain has some means of knowing which kind of cone is sending it messages. If it were achieved by genetic hard wiring this brain cell is hooked up to a red cone, that nerve cell is hooked up to a green cone the system would work, but it couldn't cope with mutations in the retina. How could it? How could brain cells be expected to 'know' that a new opsin, sensitive to a different colour, has suddenly become available and that a particular set of cones, in the huge population of cones in the retina, have turned on the gene for making the new opsin?

It seems that the only plausible answer is that the brain learns. Presumably it compares the firing rates that originate in the population of cone cells in the retina and 'notices' that one sub-population of cells fires strongly when tomatoes and strawberries are seen; another sub-population when looking at the sky; another when looking at gra.s.s. This is a 'toy' speculation, but I suppose something like it enables the nervous system swiftly to accommodate a genetic change in the retina. My colleague Colin Blakemore, with whom I raised the matter, sees this problem as one of a family of similar problems that arise whenever the central nervous system has to adjust itself to a change in the periphery.9 The final lesson of the Howler Monkey's Tale is the importance of gene duplication. The red and the green opsin genes are clearly derived from a single ancestral gene that xeroxed itself to a different part of the X chromosome. Farther back in time, we may be sure, it was a similar duplication that separated the blue10 autosomal gene from what was to become the red/green X-chromosomal gene. It is common for genes on completely different chromosomes to belong to the same 'gene family'. Gene families have arisen by ancient DNA duplications followed by divergence of function. Various studies have found that a typical human gene has an average probability of duplication of about 0.1 to 1 per cent per million years. DNA duplication can be a piecemeal affair, or it can happen in bursts, for example when a newly virulent DNA parasite like autosomal gene from what was to become the red/green X-chromosomal gene. It is common for genes on completely different chromosomes to belong to the same 'gene family'. Gene families have arisen by ancient DNA duplications followed by divergence of function. Various studies have found that a typical human gene has an average probability of duplication of about 0.1 to 1 per cent per million years. DNA duplication can be a piecemeal affair, or it can happen in bursts, for example when a newly virulent DNA parasite like Alu Alu spreads throughout the genome, or when a genome is duplicated wholesale. (Entire-genome duplication is common in plants, and is postulated to have happened at least twice in our ancestry, during the origination of the vertebrates.) Regardless of when or how it happens, accidental DNA duplication is one of the major sources of new genes. Over evolutionary time, it isn't only genes that change, within genomes. Genomes themselves change. spreads throughout the genome, or when a genome is duplicated wholesale. (Entire-genome duplication is common in plants, and is postulated to have happened at least twice in our ancestry, during the origination of the vertebrates.) Regardless of when or how it happens, accidental DNA duplication is one of the major sources of new genes. Over evolutionary time, it isn't only genes that change, within genomes. Genomes themselves change.

1 'Used' is, of course, unfortunate if it implies anything more than inadvertence. As we shall see in the Dodo's Tale, no animal ever tries to colonise brand new territory. But when it accidentally happens, the evolutionary consequences can be momentous. 'Used' is, of course, unfortunate if it implies anything more than inadvertence. As we shall see in the Dodo's Tale, no animal ever tries to colonise brand new territory. But when it accidentally happens, the evolutionary consequences can be momentous.

2 Prehensile tails are also found in several other South American groups, including kinkajous (carnivores), porcupines (rodents), tree-anteaters (xenarthrans), opossums (marsupials), and even the salamander Prehensile tails are also found in several other South American groups, including kinkajous (carnivores), porcupines (rodents), tree-anteaters (xenarthrans), opossums (marsupials), and even the salamander Bolitoglossa Bolitoglossa. Is there something special about South America? But prehensile tails also occur in pangolins, some tree rats, some skinks and chameleons not from South America!

3 This raises an intriguing possibility. Imagine that a neurobiologist inserts a tiny probe into, say, a green cone and stimulates it electrically. The green cell will now report 'light' while all other cells are silent. Will the brain 'see' a 'super green' hue such as could not possibly be achieved by any real light? Real light, no matter how pure, would always stimulate all three cla.s.ses of cones to differing extents. This raises an intriguing possibility. Imagine that a neurobiologist inserts a tiny probe into, say, a green cone and stimulates it electrically. The green cell will now report 'light' while all other cells are silent. Will the brain 'see' a 'super green' hue such as could not possibly be achieved by any real light? Real light, no matter how pure, would always stimulate all three cla.s.ses of cones to differing extents.

4 Carrots are rich in beta-carotene from which vitamin A can be made: hence the rumour rumours can be true that carrots improve vision. Carrots are rich in beta-carotene from which vitamin A can be made: hence the rumour rumours can be true that carrots improve vision.

5 Actually, red and green are only two out of a range of possibilities at this locus, but we have enough complications to be going on with. For the purposes of this tale they will be firmly 'red' and 'green'. Actually, red and green are only two out of a range of possibilities at this locus, but we have enough complications to be going on with. For the purposes of this tale they will be firmly 'red' and 'green'.

6 As for ensuring that, in any one cone, only the red or the green opsin gene, but not both, is turned on, this happens to be easy for females. They already have a mechanism for turning the whole of one X chromosome off in any cell. A random half of the cells deactivates one of the two X chromosomes, the other half the other one. This is important, because all the genes on an X chromosome are set up to work if only one is active necessary because males only have one X chromosome. As for ensuring that, in any one cone, only the red or the green opsin gene, but not both, is turned on, this happens to be easy for females. They already have a mechanism for turning the whole of one X chromosome off in any cell. A random half of the cells deactivates one of the two X chromosomes, the other half the other one. This is important, because all the genes on an X chromosome are set up to work if only one is active necessary because males only have one X chromosome.

7 This sadly affects many African-Americans, who no longer live in a malarial country but inherit the genes of ancestors who did. Another example is the debilitating disease cystic fibrosis whose gene, in the heterozygous condition, seems to confer protection against cholera. This sadly affects many African-Americans, who no longer live in a malarial country but inherit the genes of ancestors who did. Another example is the debilitating disease cystic fibrosis whose gene, in the heterozygous condition, seems to confer protection against cholera.

8 Mark Ridley, in Mark Ridley, in Mendel's Demon Mendel's Demon (ret.i.tled (ret.i.tled The Cooperative Gene The Cooperative Gene in America), points out that the eight per cent (or higher) figure applies to Europeans, and others with a history of good medicine. Hunter-gatherers, and other 'traditional' societies closer to the cutting edge of natural selection, show a lower percentage. Ridley suggests that a relaxation of natural selection has allowed colourblindness to increase. The whole business of colourblindness is treated, in characteristically original fashion, by Oliver Sacks in in America), points out that the eight per cent (or higher) figure applies to Europeans, and others with a history of good medicine. Hunter-gatherers, and other 'traditional' societies closer to the cutting edge of natural selection, show a lower percentage. Ridley suggests that a relaxation of natural selection has allowed colourblindness to increase. The whole business of colourblindness is treated, in characteristically original fashion, by Oliver Sacks in The Island of the Colour-Blind The Island of the Colour-Blind.

9 I expect that some such learning must be used by birds and reptiles, who enhance their range of colour sensitivities by planting tiny coloured oil droplets over the surface of the retina. I expect that some such learning must be used by birds and reptiles, who enhance their range of colour sensitivities by planting tiny coloured oil droplets over the surface of the retina.

10 Or ultraviolet or whatever it was in those days. Presumably the exact colour sensitivities of all these cla.s.ses of opsin have been modified over the evolutionary years anyway. Or ultraviolet or whatever it was in those days. Presumably the exact colour sensitivities of all these cla.s.ses of opsin have been modified over the evolutionary years anyway.

Rendezvous 7.

TARSIERS.

We anthropoid pilgrims have arrived at Rendezvous 7 Rendezvous 7, 58 million years ago in the dense and varied forests of the Palaeocene Epoch. There we greet a little evolutionary trickle of cousins, the tarsiers. We need a name for the clade that unites anthropoids and tarsiers, and it is haplorhines. The haplorhines consist of Concestor 7, perhaps our 6-million-greats-grandparent, and all its descendants: tarsiers, 'monkeys' and apes.

The first thing you notice about a tarsier is its eyes. Looking at the skull, it is almost the only thing there is to notice: a pair of eyes on legs pretty well sums up a tarsier. Each one of its eyes is as large as its entire brain, and the pupils open very wide too. The skull seen head-on seems to be wearing a pair of fashionably outsize, not to say giant, spectacles. Their huge size makes the eyes hard to rotate in their sockets but tarsiers, like some owls, are equal to the challenge. They rotate the whole head, on an extremely flexible neck, through nearly 360 degrees. The reason for their huge eyes is the same as in owls and night monkeys tarsiers are nocturnal. They rely on moonlight, starlight and twilight, and need to sweep up every last photon they can.

Other nocturnal mammals have a tapetum lucidum a reflecting layer behind the retina, which turns photons back in their tracks, so giving the retinal pigments a second chance to intercept them. It is the tapetum that makes it easy to spot cats and other animals at night.1 Shine a torch all around you. It will catch the attention of any animals in the vicinity, and they'll look straight at your light out of curiosity. The beam will be reflected back off the tapetum. Sometimes you can locate dozens of pairs of eyes with a single sweep of the torch. If electric light beams had been a feature of the environment in which animals evolved, they might well not have evolved a tapetum lucidum, as it is such a giveaway. Shine a torch all around you. It will catch the attention of any animals in the vicinity, and they'll look straight at your light out of curiosity. The beam will be reflected back off the tapetum. Sometimes you can locate dozens of pairs of eyes with a single sweep of the torch. If electric light beams had been a feature of the environment in which animals evolved, they might well not have evolved a tapetum lucidum, as it is such a giveaway.

Tarsiers, surprisingly, have no tapetum lucidum. It has been suggested that their ancestors, along with other primates, pa.s.sed through a diurnal phase and lost the tapetum. This is supported by the fact that tarsiers have the same weird system of colour vision as most of the New World monkeys. Several groups of mammals that were nocturnal in the time of the dinosaurs became diurnal when the death of the dinosaurs made it safe to do so. The suggestion is that the tarsiers subsequently returned to the night, but for some reason the evolutionary avenue of regrowing the tapetum was blocked to them. So they achieved the same result, of capturing as many photons as possible, by making their eyes very big indeed.2 [image]

Tarsiers join. Recent morphological and molecular studies place the five tarsier species as the sister group to the apes and monkeys, rather than allied to the lemurs as previously thought. Recent morphological and molecular studies place the five tarsier species as the sister group to the apes and monkeys, rather than allied to the lemurs as previously thought.

Image: Philippine tarsier ( Philippine tarsier (Tarsius syrichta).

[image]

The other descendants of Concestor 7, the 'monkeys' and apes, also lack a tapetum lucidum, not surprisingly given that they are all diurnal except the owl monkeys of South America. And the owl monkeys, like the tarsiers, have compensated by growing very large eyes although not quite so large, in proportion to the head, as those of the tarsiers. We can make a good guess that Concestor 7 also lacked a tapetum lucidum and was probably diurnal. What else can we say about it?

Apart from being diurnal, it may have been quite tarsier-like. The reason for saying this is that there are some plausible fossils called the omomyids dating from about the right period. Concestor 7 might have been something like an omomyid, and the omomyids were quite tarsier-like. Their eyes were not so big as modern tarsiers', but big enough to suggest that they were nocturnal. Perhaps Concestor 7 was a diurnal version of an omomyid, living in trees. Of its two descendant lineages, one stayed in the light and blossomed into the anthropoid monkeys and apes. The other reverted to the darkness and became the modern tarsiers.

Eyes apart, what is to be said about tarsiers? They are outstanding leapers, with long legs like frogs or gra.s.shoppers. A tarsier can jump more then 3 metres horizontally and 1.5 metres vertically. They have been called furry frogs. It is probably no accident that they resemble frogs too in uniting the two bones of the lower legs, the tibia and the fibula, to make a single strong bone, the tibiofibula. All anthropoids have nails instead of claws, and tarsiers do too, with the curious exception of 'grooming claws' on the second and third toes.

We can't guess with any certainty where Rendezvous 7 Rendezvous 7 takes place. But we might just note that North America is rich in early omomyid fossils of the right period, and that it was in those days firmly joined to Eurasia via what is now Greenland. Perhaps Concestor 7 was a North American. takes place. But we might just note that North America is rich in early omomyid fossils of the right period, and that it was in those days firmly joined to Eurasia via what is now Greenland. Perhaps Concestor 7 was a North American.

1 Most nocturnal birds, too, have reflecting eyes, but not the owlet nightjars (Aegothelidae) of Australasia, nor the Galapagos swallowtailed gull Most nocturnal birds, too, have reflecting eyes, but not the owlet nightjars (Aegothelidae) of Australasia, nor the Galapagos swallowtailed gull Creagrus furcatus Creagrus furcatus, the only nocturnal gull in the world.

2 On this theory, if the tarsiers had managed to regrow a tapetum they wouldn't need such huge eyes and this would have been a good thing. The absolutely largest eyes in the entire animal kingdom are those of the giant squid, nearly a foot in diameter. They too have to cope with very low light levels, this time not because they are nocturnal but because so little light penetrates to the great depths of ocean that they inhabit. On this theory, if the tarsiers had managed to regrow a tapetum they wouldn't need such huge eyes and this would have been a good thing. The absolutely largest eyes in the entire animal kingdom are those of the giant squid, nearly a foot in diameter. They too have to cope with very low light levels, this time not because they are nocturnal but because so little light penetrates to the great depths of ocean that they inhabit.

Rendezvous 8.

LEMURS, BUSHBABIES AND THEIR KIN.

Gathering the little leaping tarsiers into our pilgrimage, we head off back towards Rendezvous 8 Rendezvous 8, where we are to be joined by the rest of the primates traditionally called prosimians: the lemurs, pottos, bushbabies and lorises. We need a name for those 'prosimians' that are not tarsiers. 'Strepsirhines' has become customary. It means 'split nostril' (literally twisted nose). It is a slightly confusing name. All it means is that the nostril is shaped like a dog's. The rest of the primates, including us, are haplorhines (simple nose: our nostrils are each just a simple hole).

We haplorhine pilgrims, then, greet our strepsirhine cousins, of which the great majority are lemurs, at Rendezvous 8 Rendezvous 8. Various dates have been suggested for this point. I have taken it as 63 million years into the past, a commonly accepted date and one just 'before' our pa.s.sage back into the Cretaceous Period. Bear in mind, however, that a few researchers imagine this rendezvous even further back in time, during the Cretaceous itself. At 63 million years ago, the Earth's vegetation and climate had rebounded from their drastic disturbance when the Cretaceous and the dinosaurs came to an end (see 'The Great Cretaceous Catastrophe'). The world was largely wet and forested, with at least the northern continents covered in a relatively restricted mix of deciduous conifers, and a scattering of flowering plant species.

Perhaps in the branches of a tree, we encounter Concestor 8, seeking fruit or maybe an insect. This most recent common ancestor of all surviving primates is approximately our 7-million-greats-grandparent. Fossils that might help us reconstruct what Concestor 8 was like include the large group called plesiadapiforms. They lived about the right time, and they have many of the qualities you would expect of the grand ancestor of all the primates. Not all of them, however, which makes their supposed position close to the primate ancestor controversial.

Of the living strepsirhines, the majority are lemurs, living exclusively in Madagascar, and we'll come to them in the tale that follows. The others divide into two main groups, the leaping bushbabies and the creeping lorises and pottos. When I was a child of three in Nyasaland (now Malawi) we had a pet bushbaby. Percy was brought in by a local African, and was probably an orphaned juvenile. He was tiny: small enough to perch on the rim of a gla.s.s of whisky, into which he would dip his hand and drink with evident enjoyment. He slept during the day, clasping the underside of a beam in the bathroom. When his 'morning' came (in the evening), if my parents failed to catch him in time (which was often, because he was extremely agile and a terrific leaper) he would race to the top of my mosquito net and urinate on me from above. When leaping, for example onto a person, he did not exhibit the common bushbaby habit of urinating on his hands first. On the theory that 'urine washing' is for scent-marking, this would make sense given that he was not an adult. On the alternative theory that the urine improves grip, it is less clear why he didn't do it.

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Lemurs and their kin join. The living primates can be divided into the lemurs and their kin, and the rest. The time of this divergence is debated some experts place it as much as 20 million years earlier, with a consequent increase in the age of Concestors 9, 10, and 11. The five Madagascan lemur families (30 or so species) and the loris family (18 species) are known as 'strepsirhines'. The order of branching within lemurs in this strepsirhine phylogeny remains controversial. The living primates can be divided into the lemurs and their kin, and the rest. The time of this divergence is debated some experts place it as much as 20 million years earlier, with a consequent increase in the age of Concestors 9, 10, and 11. The five Madagascan lemur families (30 or so species) and the loris family (18 species) are known as 'strepsirhines'. The order of branching within lemurs in this strepsirhine phylogeny remains controversial.

Images, left to right: pygmy mouse lemur ( pygmy mouse lemur (Microcebus myoxinus); red-tailed sportive lemur (Lepilemur ruficaudatus); indri (Indri indri); white-fronted brown lemur (Eulemur fulvus albifrons); aye-aye (Daubentonia madagascariensis); slender loris (Loris tardigradus).

I shall never know to which of the 17 species of bushbaby Percy belonged, but he was most certainly a leaper, not a creeper. The creepers are the pottos of Africa and the lorises of Asia. They move much more slowly especially the 'slow loris' of the Far East, which is a stealth hunter, inching along a branch until within reach of prey, whereupon it lunges with great speed.

Bushbabies and pottos remind us that a tropical forest is a three-dimensional world like the sea. Seen from above the canopy, the green waves at its surface billow towards the horizon. Dive down into the darker green world beneath, and you pa.s.s through distinct layers, again as in the sea. The animals of the forest, like fish in the sea, find it as easy to move up and down as horizontally. But, also as in the sea, each species in practice specialises in making its living at a particular level. In the West African forests by night, the surface canopy is the province of the pygmy bushbabies hunting insects, and the fruit-eating pottos. Below the level of the canopy, the trunks of the trees are separated by gaps, and this is the domain of the needle-clawed bushbaby whose eponymous equipment enables it to cling to the trunks after leaping the gaps between them. Deeper still, in the understorey, the golden potto and the closely related angwantibo hunt caterpillars. At dawn, the nocturnal bushbabies and pottos give place to day-hunting monkeys, who parcel up the forest into similarly stratified layers. The same kind of stratification goes on in the South American forests, where as many as seven species of (marsupial) possum can be found, each at its own level.

The lemurs are descended from those early primates who happened to find themselves marooned in Madagascar during the time when monkeys were evolving in Africa. Madagascar is a large enough island to serve as a laboratory for natural experiments in evolution. The tale of Madagascar will be told by one of the lemurs, by no means the most typical of them, the aye-aye Daubentonia Daubentonia. I don't remember much from the discourse on lemurs that Harold Pusey wise and learned warhorse of the lecture hall gave to my generation of Oxford zoologists, but I do remember the haunting refrain with which he concluded almost every sentence about lemurs: 'Except Daubentonia Daubentonia.' 'EXCEPT Daubentonia! Daubentonia!' Despite appearances, Daubentonia Daubentonia, the aye-aye, is a perfectly respectable lemur, and lemurs are the most famous inhabitants of the great island of Madagascar. The Aye-Aye's Tale is about Madagascar, textbook showcase of biogeographical natural experiments, a tale not just of lemurs but of all of Madagascar's peculiar in the original sense of the word fauna and flora.

THE AYE-AYE'S TALE A British politician once described a rival (who later went on to become their party leader) as having 'something of the night' about him. The aye-aye conveys a similar impression, and indeed it is wholly nocturnal the largest primate to be so. It has disconcertingly wide-set eyes in a ghostly pale face. The fingers are absurdly long: the fingers of an Arthur Rackham witch. 'Absurd' only by human standards, however, for we may be sure those fingers are long for a good reason: aye-ayes with shorter fingers would be penalised by natural selection, even if we don't know why. Natural selection is a strong enough theory to be predictive in this fashion, now that science no longer needs convincing of its truth.

One finger, the middle finger, is unique. Hugely long and thin, even by aye-aye standards, it is used specifically to make holes in dead wood and lever out grubs. Aye-ayes detect prey in wood by drumming with the same long finger, and listening for the changes in tone that betra