1An uneasy tension disturbs the heart of the selfish gene theory. It is the tension between gene and individual body as fundamental agent of life.

2On the one hand we have the beguiling image of independent DNA replicators, skipping like chamois, free and untrammelled down the generations, temporarily brought together in throwaway survival machines, immortal coils shuffling off an endless succession of mortal ones as they forge towards their separate eternities. On the other hand we look at the individual bodies themselves and each one is obviously a coherent, integrated, immensely complicated machine, with a conspicuous unity of purpose. A body doesn't look like the product of a loose and temporary federation of warring genetic agents who hardly have time to get acquainted before embarking in sperm or egg for the next leg of the great genetic diaspora. It has one single-minded brain which coordinates a cooperative of limbs and sense organs to achieve one end. The body looks and behaves like a pretty impressive agent in its own right.

3In some chapters of this book we have indeed thought of the individual organism as an agent, striving to maximize its success in passing on all its genes. We imagined individual animals making complicated economic

4'as if' calculations about the genetic benefits of various courses of action.

5Yet in other chapters the fundamental rationale was presented from the point of view of genes.

6Without the gene's-eye view of life there is no particular reason why an organism should 'care' about its reproductive success and that of its relatives, rather than, for instance, its own longevity.

7How shall we resolve this paradox of the two ways of looking at life? My own attempt to do so is spelled out in The Extended Phenotype, the book that, more than anything else I have achieved in my professional life, is my pride and joy. This chapter is a brief distillation of a few of the themes in that book, but really I'd almost rather you stopped reading now and switched to The Extended Phenotype!

8On any sensible view of the matter Darwinian selection does not work on genes directly. DNA is cocooned in protein, swaddled in membranes, shielded from the world and invisible to natural selection. If selection tried to choose DNA molecules directly it would hardly find any criterion by which to do so. All genes look alike, just as all recording tapes look alike. The important differences between genes emerge only in their effects. This usually means effects on the processes of embryonic development and hence on bodily form and behaviour. Successful genes are genes that, in the environment influenced by all the other genes in a shared embryo, have beneficial effects on that embryo. Beneficial means that they make the embryo likely to develop into a successful adult, an adult likely to reproduce and pass those very same genes on to future generations. The technical word Phenotype is used for the bodily manifestation of a gene, the effect that a gene, in comparison with its alleles, has on the body, via development. The phenotypic effect of some particular gene might be, say, green eye colour. In practice most genes have more than one phenotypic effect, say green eye colour and curly hair. Natural selection favours some genes rather than others not because of the nature of the genes themselves, but because of their consequences-their phenotypic effects.

9Darwinians have usually chosen to discuss genes whose phenotypic effects benefit, or penalize, the survival and reproduction of whole bodies.

10They have tended not to consider benefits to the gene itself. This is partly why the paradox at the heart of the theory doesn't normally make itself felt. For instance a gene may be successful through improving the running speed of a predator. The whole predator's body, including all its genes, is more successful because it runs faster. Its speed helps it survive to have children; and therefore more copies of all its genes, including the gene for fast running, are passed on. Here the paradox conveniently disappears because what is good for one gene is good for all.

11But what if a gene exerted a phenotypic effect that was good for itself but bad for the rest of the genes in the body? This is not a flight of fancy.

12Cases of it are known, for instance the intriguing phenomenon called meiotic drive. Meiosis, you will remember, is the special kind of cell division that halves the number of chromosomes and gives rise to sperm cells or egg cells. Normal meiosis is a completely fair lottery. Of each pair of alleles, only one can be the lucky one that enters any given sperm or egg. But it is equally likely to be either one of the pair, and if you average over lots of sperms (or eggs) it turns out that half of them contain one allele, half the other. Meiosis is fair, like tossing a penny. But, though we proverbially think of tossing a penny as random, even that is a physical process influenced by a multitude of circumstances- the wind, precisely how hard the penny is flicked, and so on. Meiosis, too, is a physical process, and it can be influenced by genes. What if a mutant gene arose that just happened to have an effect, not upon something obvious like eye colour or curliness of hair, but upon meiosis itself? Suppose it happened to bias meiosis in such a way that it, the mutant gene itself, was more likely than its allelic partner to end up in the egg. There are such genes and they are called segregation distorters. They have a diabolical simplicity. When a segregation distorter arises by mutation, it will spread inexorably through the population at the expense of its allele.

13It is this that is known as meiotic drive. It will happen even if the effects on bodily welfare, and on the welfare of all the other genes in the body, are disastrous.

14Throughout this book we have been alert to the possibility of individual organisms 'cheating' in subtle ways against their social companions.

15Here we are talking about single genes cheating against the other genes with which they share a body.

16The geneticist James Crow has called them 'genes that beat the system'. One of the best-known segregation distorters is the so-called t gene in mice. When a mouse has two t genes it either dies young or is sterile, t is therefore said to be lethal in the homozygous state. If a male mouse has only one t gene it will be a normal, healthy mouse except in one remarkable respect. If you examine such a male's sperms you will find that up to 95 per cent of them contain the t gene, only 5 per cent the normal allele. This is obviously a gross distortion of the 50 per cent ratio that we expect. Whenever, in a wild population, a t allele happens to arise by mutation, it immediately spreads like a brushfire.

17How could it not, when it has such a huge unfair advantage in the meiotic lottery? It spreads so fast that, pretty soon, large numbers of individuals in the population inherit the t gene in double dose (that is, from both their parents). These individuals die or are sterile, and before long the whole local population is likely to be driven extinct. There is some evidence that wild populations of mice have, in the past, gone extinct through epidemics of t genes.

18Not all segregation distorters have such destructive side-effects as t.

19Nevertheless, most of them have at least some adverse consequences.

20(Almost all genetic side-effects are bad, and a new mutation will normally spread only if its bad effects are outweighed by its good effect. If both good and bad effects apply to the whole body, the net effect can still be good for the body. But if the bad effects are on the body, and the good effects are on the gene alone, from the body's point of view the net effect is all bad.) In spite of its deleterious side-effects, if a segregation distorter arises by mutation it will surely tend to spread through the population.

21Natural selection (which, after all, works at the genic level) favours the segregation distorter, even though its effects at the level of the individual organism are likely to be bad.

22Although segregation distorters exist they aren't very common. We could go on to ask why they aren't common, which is another way of asking why the process of meiosis is normally fair, as scrupulously impartial as tossing a good penny. We'll find that the answer drops out once we have understood why organisms exist anyway.

23The individual organism is something whose existence most biologists take for granted, probably because its parts do pull together in such a united and integrated way. Questions about life are conventionally questions about organisms. Biologists ask why organisms do this, why organisms do that. They frequently ask why organisms group themselves into societies. They don't ask-though they should-why living matter groups itself into organisms in the first place. Why isn't the sea still a primordial battleground of free and independent replicators? Why did the ancient replicators club together to make, and reside in, lumbering robots, and why are those robots-individual bodies, you and me-so large and so complicated?

24It is hard for many biologists even to see that there is a question here at all. This is because it is second nature for them to pose their questions at the level of the individual organism. Some biologists go so far as to see DNA as a device used by organisms to reproduce themselves, just as an eye is a device used by organisms to see! Readers of this book will recognize that this attitude is an error of great profundity. It is the truth turned crashingly on its head. They will also recognize that the alternative attitude, the selfish gene view of life, has a deep problem of its own. That problem-almost the reverse one-is why individual organisms exist at all, especially in a form so large and coherently purposeful as to mislead biologists into turning the truth upside down. To solve our problem, we have to begin by purging our minds of old attitudes that covertly take the individual organism for granted; otherwise we shall be begging the question. The instrument with which we shall purge our minds is the idea that I call the extended phenotype. It is to this, and what it means, that I now turn.

25The phenotypic effects of a gene are normally seen as all the effects that it has on the body in which it sits. This is the conventional definition.

26But we shall now see that the phenotypic effects of a gene need to be thought of as all the effects that it has on the world. It may be that a gene's effects, as a matter of fact, turn out to be confined to the succession of bodies in which the gene sits. But, if so, it will be just as a matter of fact. It will not be something that ought to be part of our very definition. In all this, remember that the phenotypic effects of a gene are the tools by which it levers itself into the next generation. All that I am going to add is that the tools may reach outside the individual body wall.

27What might it mean in practice to speak of a gene as having an extended phenotypic effect on the world outside the body in which it sits?

28Examples that spring to mind are artefacts like beaver dams, bird nests and caddis houses.

29Caddis flies are rather nondescript, drab brown insects, which most of us fail to notice as they fly rather clumsily over rivers. That is when they are adults. But before they emerge as adults they have a rather longer incarnation as larvae walking about the river bottom. And caddis larvae are anything but nondescript. They are among the most remarkable creatures on earth. Using cement of their own manufacture, they skilfully build tubular houses for themselves out of materials that they pick up from the bed of the stream. The house is a mobile home, carried about as the caddis walks, like the shell of a snail or hermit crab except that the animal builds it instead of growing it or finding it. Some species of caddis use sticks as building materials, others fragments of dead leaves, others small snail shells.

30But perhaps the most impressive caddis houses are the ones built in local stone. The caddis chooses its stones carefully, rejecting those that are too large or too small for the current gap in the wall, even rotating each stone until it achieves the snuggest fit.

31Incidentally, why does this impress us so? If we forced ourselves to think in a detached way we surely ought to be more impressed by the architecture of the caddis's eye, or of its elbow joint, than by the comparatively modest architecture of its stone house. After all, the eye and the elbow joint are far more complicated and 'designed' than the house. Yet, perhaps because the eye and elbow joint develop in the same kind of way as our own eyes and elbows develop, a building process for which we, inside our mothers, claim no credit, we are illogically more impressed by the house.

32Having digressed so far, I cannot resist going a little further. Impressed as we may be by the caddis house, we are nevertheless, paradoxically, less impressed than we would be by equivalent achievements in animals closer to ourselves. Just imagine the banner headlines if a marine biologist were to discover a species of dolphin that wove large, intricately meshed fishing nets, twenty dolphin-lengths in diameter! Yet we take a spider web for granted, as a nuisance in the house rather than as one of the wonders of the world. And think of the furore if Jane Goodall returned from Gombe stream with photographs of wild chimpanzees building their own houses, well roofed and insulated, of painstakingly selected stones neatly bonded and mortared! Yet caddis larvae, who do precisely that, command only passing interest. It is sometimes said, as though in defence of this double standard, that spiders and caddises achieve their feats of architecture by 'instinct'. But so what? In a way this makes them all the more impressive.

33Let us get back to the main argument. The caddis house, nobody could doubt, is an adaptation, evolved by Darwinian selection. It must have been favoured by selection, in very much the same way as, say, the hard shell of lobsters was favoured. It is a protective covering for the body. As such it is of benefit to the whole organism and all its genes. But we have now taught ourselves to see benefits to the organism as incidental, as far as natural selection is concerned. The benefits that actually count are the benefits to those genes that give the shell its protective properties. In the case of the lobster this is the usual story. The lobster's shell is obviously a part of its body. But what about the caddis house?

34Natural selection favoured those ancestral caddis genes that caused their possessors to build effective houses. The genes worked on behaviour, presumably by influencing the embryonic development of the nervous system. But what a geneticist would actually see is the effect of genes on the shape and other properties of houses. The geneticist should recognize genes 'for' house shape in precisely the same sense as there are genes for, say, leg shape. Admittedly, nobody has actually studied the genetics of caddis houses. To do so you would have to keep careful pedigree records of caddises bred in captivity, and breeding them is difficult. But you don't have to study genetics to be sure that there are, or at least once were, genes influencing differences between caddis houses. All you need is good reason to believe that the caddis house is a Darwinian adaptation. In that case there must have been genes controlling variation in caddis houses, for selection cannot produce adaptations unless there are hereditary differences among which to select.

35Although geneticists may think it an odd idea, it is therefore sensible for us to speak of genes 'for' stone shape, stone size, stone hardness and so on. Any geneticist who objects to this language must, to be consistent, object to speaking of genes for eye colour, genes for wrinkling in peas and so on. One reason the idea might seem odd in the case of stones is that stones are not living material. Moreover, the influence of genes upon stone properties seems especially indirect. A geneticist might wish to claim that the direct influence of the genes is upon the nervous system that mediates the stone- choosing behaviour, not upon the stones themselves. But I invite such a geneticist to look carefully at what it can ever mean to speak of genes exerting an influence on a nervous system.

36All that genes can really influence directly is protein synthesis. A gene's influence upon a nervous system, or, for that matter, upon the colour of an eye or the wrinkliness of a pea, is always indirect.

37The gene determines a protein sequence that influences X that influences Y that influences Z that eventually influences the wrinkliness of the seed or the cellular wiring up of the nervous system. The caddis house is only a further extension of this kind of sequence. Stone hardness is an extended phenotypic effect of the caddis's genes. If it is legitimate to speak of a gene as affecting the wrinkliness of a pea or the nervous system of an animal (all geneticists think it is) then it must also be legitimate to speak of a gene as affecting the hardness of the stones in a caddis house. Startling thought, isn't it? Yet the reasoning is inescapable.

38We are ready for the next step in the argument: genes in one organism can have extended phenotypic effects on the body of another organism.

39Caddis houses helped us take the previous step; snail shells will help us take this one. The shell plays the same role for a snail as the stone house does for a caddis larva. It is secreted by the snail's own cells, so a conventional geneticist would be happy to speak of genes 'for' shell qualities such as shell thickness. But it turns out that snails parasitized by certain kinds of fluke (flatworm) have extra-thick shells. What can this thickening mean? If the parasitized snails had had extra-thin shells, we'd happily explain this as an obvious debilitating effect on the snail's constitution. But a thicker shell? A thicker shell presumably protects the snail better. It looks as though the parasites are actually helping their host by improving its shell. But are they?

40We have to think more carefully. If thicker shells are really better for the snail, why don't they have them anyway? The answer probably lies in economics. Making a shell is costly for a snail. It requires energy. It requires calcium and other chemicals that have to be extracted from hard-won food. All these resources, if they were not spent on making shell substance, could be spent on something else such as making more offspring. A snail that spends lots of resources on making an extra-thick shell has bought safety for its own body. But at what cost? It may live longer, but it will be less successful at reproducing and may fail to pass on its genes. Among the genes that fail to be passed on will be the genes for making extra-thick shells. In other words, it is possible for a shell to be too thick as well as (more obviously) too thin. So, when a fluke makes a snail secrete an extra-thick shell, the fluke is not doing the snail a good turn unless the fluke is bearing the economic cost of thickening the shell.

41And we can safely bet that it isn't being so generous. The fluke is exerting some hidden chemical influence on the snail that forces the snail to shift away from its own 'preferred' thickness of shell. It may be prolonging the snail's life. But it is not helping the snail's genes.

42What is in it for the fluke? Why does it do it? My conjecture is the following. Both snail genes and fluke genes stand to gain from the snail's bodily survival, all other things being equal. But survival is not the same thing as reproduction and there is likely to be a trade-off. Whereas snail genes stand to gain from the snail's reproduction, fluke genes don't. This is because any given fluke has no particular expectation that its genes will be housed in its present host's offspring. They might be, but so might those of any of its fluke rivals. Given that snail longevity has to be bought at the cost of some loss in the snail's reproductive success, the fluke genes are 'happy' to make the snail pay that cost, since they have no interest in the snail's reproducing itself. The snail genes are not happy to pay that cost, since their long-term future depends upon the snail reproducing.

43So, I suggest that fluke genes exert an influence on the shell-secreting cells of the snail, an influence that benefits themselves but is costly to the snail's genes. This theory is testable, though it hasn't been tested yet.

44We are now in a position to generalize the lesson of the caddises. If I am right about what the fluke genes are doing, it follows that we can legitimately speak of fluke genes as influencing snail bodies, in just the same sense as snail genes influence snail bodies. It is as if the genes reached outside their 'own' body and manipulated the world outside. As in the case of the caddises, this language might make geneticists uneasy.

45They are accustomed to the effects of a gene being limited to the body in which it sits. But, again as in the case of the caddises, a close look at what geneticists ever mean by a gene having 'effects' shows that such uneasiness is misplaced. We need to accept only that the change in snail shell is a fluke adaptation. If it is, it has to have come about by Darwinian selection of fluke genes. We have demonstrated that the phenotypic effects of a gene can extend, not only to inanimate objects like stones, but to 'other' living bodies too.

46The story of the snails and flukes is only the beginning. Parasites of all types have long been known to exert fascinatingly insidious influences on their hosts. A species of microscopic protozoan parasite called Nosema, which infests the larvae of flour beetles, has 'discovered' how to manufacture a chemical that is very special for the beetles. Like other insects, these beetles have a hormone called the juvenile hormone which keeps larvae as larvae. The normal change from larva to adult is triggered by the larva ceasing production of juvenile hormone. The parasite Nosema has succeeded in synthesizing (a close chemical analogue of) this hormone. Millions of Nosema club together to mass- produce juvenile hormone in the beetle larva's body, thereby preventing it from turning into an adult.

47Instead it goes on growing, ending up as a giant larva more than twice the weight of a normal adult.

48No good for propagating beetle genes, but a cornucopia for Nosema parasites. Giantism in beetle larvae is an extended phenotypic effect of protozoan genes.

49And here is a case history to provoke even more Freudian anxiety than the Peter Pan beetles-parasitic castration! Crabs are parasitized by a creature called Sacculina. Sacculina is related to barnacles, though you would think, to look at it, that it was a parasitic plant. It drives an elaborate root system deep into the tissues of the unfortunate crab, and sucks nourishment from its body. It is probably no accident that among the first organs that it attacks are the crab's testicles or ovaries; it spares the organs that the crab needs to survive-as opposed to reproduce-till later. The crab is effectively castrated by the parasite. Like a fattened bullock, the castrated crab diverts energy and resources away from reproduction and into its own body-rich pickings for the parasite at the expense of the crab's reproduction. Very much the same story as I conjectured for Nosema in the flour beetle and for the fluke in the snail.

50In all three cases the changes in the host, if we accept that they are Darwinian adaptations for the benefit of the parasite, must be seen as extended phenotypic effects of parasite genes. Genes, then, reach outside their 'own' body to influence phenotypes in other bodies.

51To quite a large extent the interests of parasite genes and host genes may coincide. From the selfish gene point of view we can think of both fluke genes and snail genes as 'parasites' in the snail body.

52Both gain from being surrounded by the same protective shell, though they diverge from one another in the precise thickness of shell that they 'prefer'. This divergence arises, fundamentally, from the fact that their method of leaving this snail's body and entering another one is different. For the snail genes the method of leaving is via snail sperms or eggs. For the fluke's genes it is very different. Without going into the details (they are distractingly complicated) what matters is that their genes do not leave the snail's body in the snail's sperms or eggs.

53I suggest that the most important question to ask about any parasite is this. Are its genes transmitted to future generations via the same vehicles as the host's genes? If they are not, I would expect it to damage the host, in one way or another. But if they are, the parasite will do all that it can to help the host, not only to survive but to reproduce. Over evolutionary time it will cease to be a parasite, will cooperate with the host, and may eventually merge into the host's tissues and become unrecognizable as a parasite at all. Maybe, as I suggested earlier, our cells have come far across this evolutionary spectrum: we are all relics of ancient parasitic mergers.

54Look at what can happen when parasite genes and host genes do share a common exit. Wood-boring ambrosia beetles (of the species Xyleborus ferrugineus) are parasitized by bacteria that not only live in their host's body but also use the host's eggs as their transport into a new host. The genes of such parasites therefore stand to gain from almost exactly the same future circumstances as the genes of their host. The two sets of genes can be expected to 'pull together' for just the same reasons as all the genes of one individual organism normally pull together. It is irrelevant that some of them happen to be 'beetle genes', while others happen to be 'bacterial genes'. Both sets of genes are 'interested' in beetle survival and the propagation of beetle eggs, because both 'see' beetle eggs as their passport to the future. So the bacterial genes share a common destiny with their host's genes, and in my interpretation we should expect the bacteria to cooperate with their beetles in all aspects of life.

55It turns out that 'cooperate' is putting it mildly. The service they perform for the beetles could hardly be more intimate. These beetles happen to be haplodiploid, like bees and ants (see Chapter 10). If an egg is fertilized by a male, it always develops into a female. An unfertilized egg develops into a male. Males, in other words, have no father. The eggs that give rise to them develop spontaneously, without being penetrated by a sperm. But, unlike the eggs of bees and ants, ambrosia beetle eggs do need to be penetrated by something. This is where the bacteria come in. They prick the unfertilized eggs into action, provoking them to develop into male beetles. These bacteria are, of course, just the kind of parasites that, I argued, should cease to be parasitic and become mutualistic, precisely because they are transmitted in the eggs of the host, together with the host's 'own' genes. Ultimately, their 'own' bodies are likely to disappear, merging into the 'host' body completely.

56A revealing spectrum can still be found today among species of hydra-small, sedentary, tentacled animals, like freshwater sea anemones. Their tissues tend to be parasitized by algae. (The 'g' should be pronounced hard. For unknown reasons some biologists, not least in America, have recently taken to saying Algy as in Algernon, not only for the plural 'algae', which is-just-forgivable, but also for the singular 'alga', which is not.) In the species Hydra vulgaris and Hydra attenuata, the algae are real parasites of the hydras, making them ill. In Chlorohydra viridissitnay on the other hand, the algae are never absent from the tissues of the hydras, and make a useful contribution to their well-being, providing them with oxygen. Now here is the interesting point. Just as we should expect, in Chlorohydra the algae transmit themselves to the next generation by means of the hydra's egg. In the other two species they do not. The interests of alga genes and Chlorohydra genes coincide. Both are interested in doing everything in their power to increase production of Chlorohydra eggs. But the genes of the other two species of hydra do not 'agree' with the genes of their algae. Not to the same extent, anyway.

57Both sets of genes may have an interest in the survival of hydra bodies.

58But only hydra genes care about hydra reproduction. So the algae hang on as debilitating parasites rather than evolving towards benign cooperation. The key point, to repeat it, is that a parasite whose genes aspire to the same destiny as the genes of its host shares all the interests of its host and will eventually cease to act parasitically.

59Destiny, in this case, means future generations. Chlorohydra genes and alga genes, beetle genes and bacteria genes, can get into the future only via the host's eggs. Therefore, whatever 'calculations' the parasite genes make about optimal policy, in any department of life, will converge on exactly, or nearly exactly, the same optimal policy as similar 'calculations' made by host genes. In the case of the snail and its fluke parasites, we decided that their preferred shell thicknesses were divergent. In the case of the ambrosia beetle and its bacteria, host and parasite will agree in preferring the same wing length, and every other feature of the beetle's body. We can predict this without knowing any details of exactly what the beetles might use their wings, or anything else, for. We can predict it simply from our reasoning that both the beetle genes and the bacterial genes will take whatever steps lie in their power to engineer the same future events- events favourable to the propagation of beetle eggs.

60We can take this argument to its logical conclusion and apply it to normal, 'own' genes. Our own genes cooperate with one another, not because they are our own but because they share the same outlet- sperm or egg-into the future. If any genes of an organism, such as a human, could discover a way of spreading themselves that did not depend on the conventional sperm or egg route, they would take it and be less cooperative. This is because they would stand to gain by a different set of future outcomes from the other genes in the body. We've already seen examples of genes that bias meiosis in their own favour. Perhaps there are also genes that have broken out of the sperm/egg 'proper channels' altogether and pioneered a sideways route.

61There are fragments of DNA that are not incorporated in chromosomes but float freely and multiply in the fluid contents of cells, especially bacterial cells. They go under various names such as viroids or plasmids.

62A plasmid is even smaller than a virus, and it normally consists of only a few genes. Some plasmids are capable of splicing themselves seamlessly into a chromosome. So smooth is the splice that you can't see the join: the plasmid is indistinguishable from any other part of the chromosome.

63The same plasmids can also cut themselves out again. This ability of DNA to cut and splice, to jump in and out of chromosomes at the drop of a hat, is one of the more exciting facts that have come to light since the first edition of this book was published. From some points of view it does not really matter whether these fragments originated as invading parasites or breakaway rebels. Their likely behaviour will be the same. I shall talk about a breakaway fragment in order to emphasize my point.

64Consider a rebel stretch of human DNA that is capable of snipping itself out of its chromosome, floating freely in the cell, perhaps multiplying itself up into many copies, and then splicing itself into another chromosome. What unorthodox alternative routes into the future could such a rebel replicator exploit? We are losing cells continually from our skin; much of the dust in our houses consists of our sloughed-off cells.

65We must be breathing in one another's cells all the time. If you draw your fingernail across the inside of your mouth it will come away with hundreds of living cells. The kisses and caresses of lovers must transfer multitudes of cells both ways. A stretch of rebel DNA could hitch a ride in any of these cells.

66If genes could discover a chink of an unorthodox route through to another body (alongside, or instead of, the orthodox sperm or egg route), we must expect natural selection to favour their opportunism and improve it. As for the precise methods that they use, there is no reason why these should be any different from the machinations-all too predictable to a selfish gene/extended phenotype theorist-of viruses.

67When we have a cold or a cough, we normally think of the symptoms as annoying byproducts of the virus's activities. But in some cases it seems more probable that they are deliberately engineered by the virus to help it to travel from one host to another. Not content with simply being breathed into the atmosphere, the virus makes us sneeze or cough explosively. The rabies virus is transmitted in saliva when one animal bites another. In dogs, one of the symptoms of the disease is that normally peaceful and friendly animals become ferocious biters, foaming at the mouth. Ominously too, instead of staying within a mile or so of home like normal dogs, they turn into restless wanderers, propagating the virus far afield. It has even been suggested that the well-known hydrophobic symptom encourages the dog to shake the wet foam from its mouth-and with it the virus. I do not know of any direct evidence that sexually transmitted diseases increase the libido of sufferers, but I conjecture that it would be worth looking into. Certainly at least one alleged aphrodisiac, Spanish Fly, is said to work by inducing an itch . . .

68and making people itch is just the kind of thing viruses are good at.

69The point of comparing rebel human DNA with invading parasitic viruses is that there really isn't any important difference between them. Viruses may well, indeed, have originated as collections of breakaway genes. If we want to erect any distinction, it should be between genes that pass from body to body via the orthodox route of sperms or eggs, and genes that pass from body to body via unorthodox, 'sideways' routes. Both classes may include genes that originated as 'own' chromosomal genes. And both classes may include genes that originated as external, invading parasites.

70Or perhaps all 'own' chromosomal genes should be regarded as mutually parasitic on one another.

71The important difference between my two classes of genes lies in the divergent circumstances from which they stand to benefit in the future. A cold virus gene and a breakaway human chromosomal gene agree with one another in 'wanting' their host to sneeze. An orthodox chromosomal gene and a venereally transmitted virus agree with one another in wanting their host to copulate. It is an intriguing thought that both would want the host to be sexually attractive. More, an orthodox chromosomal gene and a virus that is transmitted inside the host's egg would agree in wanting the host to succeed not just in its courtship but in every detailed aspect of its life, down to being a loyal, doting parent and even grandparent.

72The caddis lives inside its house, and the parasites that I have so far discussed have lived inside their hosts. The genes, then, are physically close to their extended phenotypic effects, as close as genes ordinarily are to their conventional phenotypes. But genes can act at a distance; extended phenotypes can extend a long way. One of the longest that I can think of spans a lake. Like a spider web or a caddis house, a beaver dam is among the true wonders of the world.

73It is not entirely clear what its Darwinian purpose is, but it certainly must have one, for the beavers expend so much time and energy to build it. The lake that it creates probably serves to protect the beaver's lodge from predators. It also provides a convenient waterway for travelling and for transporting logs. Beavers use flotation for the same reason as Canadian lumber companies use rivers and eighteenth-century coal merchants used canals. Whatever its benefits, a beaver lake is a conspicuous and characteristic feature of the landscape. It is a phenotype, no less than the beaver's teeth and tail, and it has evolved under the influence of Darwinian selection. Darwinian selection has to have genetic variation to work on. Here the choice must have been between good lakes and less good lakes. Selection favoured beaver genes that made good lakes for transporting trees, just as it favoured genes that made good teeth for felling them. Beaver lakes are extended phenotypic effects of beaver genes, and they can extend over several hundreds of yards. A long reach indeed!

74Parasites, too, don't have to live inside their hosts; their genes can express themselves in hosts at a distance. Cuckoo nestlings don't live inside robins or reed-warblers; they don't suck their blood or devour their tissues, yet we have no hesitation in labelling them as parasites.

75Cuckoo adaptations to manipulate the behaviour of foster-parents can be looked upon as extended phenotypic action at a distance by cuckoo genes.

76It is easy to empathize with foster parents duped into incubating the cuckoo's eggs. Human egg collectors, too, have been fooled by the uncanny resemblance of cuckoo eggs to, say, meadow-pipit eggs or reed-warbler eggs (different races of female cuckoos specialize in different host species).

77What is harder to understand is the behaviour of foster-parents later in the season, towards young cuckoos that are almost fledged. The cuckoo is usually much larger, in some cases grotesquely larger, than its

78'parent'. I am looking at a photograph of an adult dunnock, so small in comparison to its monstrous foster-child that it has to perch on its back in order to feed it. Here we feel less sympathy for the host.

79We marvel at its stupidity, its gullibility. Surely any fool should be able to see that there is something wrong with a child like that.

80I think that cuckoo nestlings must be doing rather more than just 'fooling' their hosts, more than just pretending to be something that they aren't. They seem to act on the host's nervous system in rather the same way as an addictive drug. This is not so hard to sympathize with, even for those with no experience of addictive drugs. A man can be aroused, even to erection, by a printed photograph of a woman's body. He is not 'fooled' into thinking that the pattern of printing ink really is a woman.

81He knows that he is only looking at ink on paper, yet his nervous system responds to it in the same kind of way as it might respond to a real woman. We may find the attractions of a particular member of the opposite sex irresistible, even though the better judgment of our better self tells us that a liaison with that person is not in anyone's long-term interests. The same can be true of the irresistible attractions of unhealthy food. The dunnock probably has no conscious awareness of its long-term best interests, so it is even easier to understand that its nervous system might find certain kinds of stimulation irresistible.

82So enticing is the red gape of a cuckoo nestling that it is not uncommon for ornithologists to see a bird dropping food into the mouth of a baby cuckoo sitting in some other bird's nest! A bird may be flying home, carrying food for its own young. Suddenly, out of the corner of its eye, it sees the red super- gape of a young cuckoo, in the nest of a bird of some quite different species. It is diverted to the alien nest where it drops into the cuckoo's mouth the food that had been destined for its own young.

83The 'irresistibility theory' fits with the views of early German ornithologists who referred to foster- parents as behaving like 'addicts'

84and to the cuckoo nestling as their 'vice'. It is only fair to add that this kind of language finds less favour with some modern experimenters. But there's no doubt that if we do assume that the cuckoo's gape is a powerful drug-like super-stimulus, it becomes very much easier to explain what is going on.

85It becomes easier to sympathize with the behaviour of the diminutive parent standing on the back of its monstrous child. It is not being stupid. 'Fooled' is the wrong word to use. Its nervous system is being controlled, as irresistibly as if it were a helpless drug addict, or as if the cuckoo were a scientist plugging electrodes into its brain.

86But even if we now feel more personal sympathy for the manipulated foster-parent, we can still ask why natural selection has allowed the cuckoos to get away with it. Why haven't host nervous systems evolved resistance to the red gape drug? Maybe selection hasn't yet had time to do its work. Perhaps cuckoos have only in recent centuries started parasitizing their present hosts, and will in a few centuries be forced to give them up and victimize other species.

87There is some evidence to support this theory. But I can't help feeling that there must be more to it than that.

88In the evolutionary 'arms race' between cuckoos and any host species, there is a sort of built-in unfairness, resulting from unequal costs of failure. Each individual cuckoo nestling is descended from a long line of ancestral cuckoo nestlings, every single one of whom must have succeeded in manipulating its foster-parent. Any cuckoo nestling that lost its hold, even momentarily, over its host would have died as a result.

89But each individual foster-parent is descended from a long line of ancestors many of whom never encountered a cuckoo in their lives. And those that did have a cuckoo in their nest could have succumbed to it and still lived to rear another brood next season. The point is that there is an asymmetry in the cost of failure. Genes for failure to resist enslavement by cuckoos can easily be passed down the generations of robins or dunnocks. Genes for failure to enslave foster-parents cannot be passed down the generations of cuckoos. This is what I meant by 'built-in unfairness', and by 'asymmetry in the cost of failure'. The point is summed up in one of Aesop's fables: 'The rabbit runs faster than the fox, because the rabbit is running for his life while the fox is only running for his dinner.' My colleague John Krebs and I have dubbed this the 'life/ dinner principle'.