The Selfish Gene Read online

  Incidentally, 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.

  Having 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.

  Let 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?

  Natural 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.

  Although 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. All 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. The 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.

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

  We 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. And 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.

  What 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.

  So, 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.

  We 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 langu
age might make geneticists uneasy. They 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.

  The 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. Instead it goes on growing, ending up as a giant larva more than twice the weight of a normal adult. No good for propagating beetle genes, but a cornucopia for Nosema parasites. Giantism in beetle larvae is an extended phenotypic effect of protozoan genes.

  And 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. In 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.

  To 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. Both 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.

  I 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.

  Look 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.

  It 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.

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

  Destiny, 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 l
ie in their power to engineer the same future events-events favourable to the propagation of beetle eggs.

  We 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.

  There 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. A 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. The 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.