The Selfish Gene

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by Richard Dawkins


  Consider 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. We 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. If 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.

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

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

  The 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.

  It 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!

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

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

  I 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. He 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.

  So 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. The 'irresistibility theory' fits with the views of early German ornithologists who referred to foster-parents as behaving like 'addicts' and 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. It 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 th
e 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.

  But 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.

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

  In 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. But 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'.

  Because of the life/dinner principle, animals might at times behave in ways that are not in their own best interests, manipulated by some other animal. Actually, in a sense they are acting in their own best interests: the whole point of the life/dinner principle is that they theoretically could resist manipulation but it would be too costly to do so. Perhaps to resist manipulation by a cuckoo you need bigger eyes or a bigger brain, which would have overhead costs. Rivals with a genetic tendency to resist manipulation would actually be less successful in passing on genes, because of the economic costs of resisting.

  But we have once again slipped back into looking at life from the point of view of the individual organism rather than its genes. When we talked about flukes and snails we accustomed ourselves to the idea that a parasite's genes could have phenotypic effects on the host's body, in exactly the same way as any animal's genes have phenotypic effects on its 'own' body. We showed that the very idea of an 'own' body was a loaded assumption. In one sense, all the genes in a body are 'parasitic' genes, whether we like to call them the body's 'own' genes or not. Cuckoos came into the discussion as an example of parasites not living inside the bodies of their hosts. They manipulate their hosts in much the same way as internal parasites do, and the manipulation, as we have now seen, can be as powerful and irresistible as any internal drug or hormone. As in the case of internal parasites, we should now rephrase the whole matter in terms of genes and extended phenotypes.

  In the evolutionary arms race between cuckoos and hosts, advances on each side took the form of genetic mutations arising and being favoured by natural selection. Whatever it is about the cuckoo's gape that acts like a drug on the host's nervous system, it must have originated as a genetic mutation. This mutation worked via its effect on, say, the colour and shape of the young cuckoo's gape. But even this was not its most immediate effect. Its most immediate effect was upon unseen chemical happenings inside cells.

  The effect of genes on colour and shape of gape is itself indirect. And now here is the point. Only a little more indirect is the effect of the same cuckoo genes on the behaviour of the besotted host. In exactly the same sense as we may speak of cuckoo genes having (phenotypic)effects on the colour and shape of cuckoo gapes, so we may speak of cuckoo genes having (extended phenotypic) effects on host behaviour. Parasite genes can have effects on host bodies, not just when the parasite lives inside the host where it can manipulate by direct chemical means, but when the parasite is quite separate from the host and manipulates it from a distance. Indeed, as we are about to see, even chemical influences can act outside the body.

  Cuckoos are remarkable and instructive creatures. But almost any wonder among the vertebrates can be surpassed by the insects. They have the advantage that there are just so many of them; my colleague Robert May has aptly observed that 'to a good approximation, all species are insects.' Insect 'cuckoos' defy listing; they are so numerous and their habit has been reinvented so often. Some examples that we'll look at have gone beyond familiar cuckooism to fulfil the wildest fantasies that The Extended Phenotype might have inspired.

  A bird cuckoo deposits her egg and disappears. Some ant cuckoo females make their presence felt in more dramatic fashion. I don't often give Latin names, but Bothriomyrmex regicidus and B. decapitans tell a story. These two species are both parasites on other species of ants. Among all ants, of course, the young are normally fed not by parents but by workers, so it is workers that any would-be cuckoo must fool or manipulate. A useful first step is to dispose of the workers' own mother with her propensity to produce competing brood. In these two species the parasite queen, all alone, steals into the nest of another ant species. She seeks out the host queen, and rides about on her back while she quietly performs, to quote Edward Wilson's artfully macabre understatement, 'the one act for which she is uniquely specialized: slowly cutting off the head of her victim'. The murderess is then adopted by the orphaned workers, who unsuspectingly tend her eggs and larvae. Some are nurtured into workers themselves, who gradually replace the original species in the nest. Others become queens who fly out to seek pastures new and royal heads yet unsevered.

  But sawing off heads is a bit of a chore. Parasites are not accustomed to exerting themselves if they can coerce a stand-in. My favourite character in Wilson's The Insect Societies is Monomorium santschii. This species, over evolutionary time, has lost its worker caste altogether. The host workers do everything for their parasites, even the most terrible task of all. At the behest of the invading parasite queen, they actually perform the deed of murdering their own mother. The usurper doesn't need to use her jaws. She uses mind-control. How she does it is a mystery; she probably employs a chemical, for ant nervous systems-are generally highly attuned to them. If her weapon is indeed chemical, then it is as insidious a drug as any known to science. For think what it accomplishes. It floods the brain of the worker ant, grabs the reins of her muscles, woos her from deeply ingrained duties and turns her against her own mother. For ants, matricide is an act of special genetic madness and formidable indeed must be the drug that drives them to it. In the world of the extended phenotype, ask not how an animal's behaviour benefits its genes; ask instead whose genes it is benefiting.

  It is hardly surprising that ants are exploited by parasites, not just other ants but an astonishing menagerie of specialist hangers-on. Worker ants sweep a rich flow of food from a wide catchment area into a central hoard which is a sitting target for freeloaders. Ants are also good agents of protection: they are well-armed and numerous. The aphids of Chapter 10 could be seen as paying out nectar to hire professional bodyguards. Several butterfly species live out their caterpillar stage inside an ants' nest Some are straightforward pillagers. Others offer something to the ants in return for protection.

  Often they bristle, literally, with equipment for manipulating their protectors. The caterpillar of a butterfly called Thisbe irenea has a sound-producing organ in its head for summoning ants, and a pair of telescopic spouts near its rear end which exude seductive nectar. On its shoulders stands another pair of nozzles, which cast an altogether more subtle
spell. Their secretion seems to be not food but a volatile potion that has a dramatic impact upon the ants' behaviour. An ant coming under the influence leaps clear into the air. Its jaws open wide and it turns aggressive, far more eager than usual to attack, bite and sting any moving object. Except, significantly, the caterpillar responsible for drugging it. Moreover, an ant under the sway of a dope-peddling caterpillar eventually enters a state called binding', in which it becomes inseparable from its caterpillar for a period of many days. Like an aphid, then, the caterpillar employs ants as bodyguards, but it goes one better. Whereas aphids rely on the ants' normal aggression against predators, the caterpillar administers an aggression-arousing drug and it seems to slip them something addictively binding as well.

  I have chosen extreme examples. But, in more modest ways, nature teems with animals and plants that manipulate others of the same or of different species. In all cases in which natural selection has favoured genes for manipulation, it is legitimate to speak of those same genes as having (extended phenotypic) effects on the body of the manipulated organism. It doesn't matter in which body a gene physically sits. The target of its manipulation may be the same body or a different one. Natural selection favours those genes that manipulate the world to ensure their own propagation. This leads to what I have called the Central Theorem of the Extended Phenotype: An animals behaviour tends to maximize the survival of the genes 'for' that behaviour, whether or not those genes happen to be in the body of the particular animal performing it. I was writing in the context of animal behaviour, but the theorem could apply, of course, to colour, size, shape-to anything.

  It is finally time to return to the problem with which we started, to the tension between individual organism and gene as rival candidates for the central role in natural selection. In earlier chapters I made the assumption that there was no problem, because individual reproduction was equivalent to gene survival. I assumed there that you can say either The organism works to propagate all its genes' or 'The genes work to force a succession of organisms to propagate them.' They seemed like two equivalent ways of saying the same thing, and which form of words you chose seemed a matter of taste. But somehow the tension remained.

 

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