The Selfish Gene - Richard Dawkins

W H Y A R E P E O P L E ?

An apparently altruistic act is one that looks, superficially, as if it must tend to make the altruist more likely (however slightly) to die, and the recipient more likely to survive. It often turns out on closer inspection that acts of apparent altruism are really selfishness in disguise. Once again, I do not mean that the underlying motives are secretly selfish, but that the real effects of the act on survival prospects are the reverse of what we originally thought.

Recently there has been a reaction against racialism and patriotism, and a tendency to substitute the whole human species as the object of our fellow feeling. This humanist broadening of the target of our altruism has an interesting corollary, which again seems to buttress the 'good of the species' idea in evolution. The politically liberal, who are normally the most convinced spokesmen of the species ethic, now often have the greatest scorn for those who have gone a little further in widening their altruism, so that it includes other species. If I say that I am more interested in preventing the slaughter of large whales than I am in improving housing conditions for people, I am likely to shock some of my friends.

The feeling that members of one's own species deserve special moral consideration as compared with members of other species is old and deep. Killing people outside war is the most seriously regarded crime ordinarily committed. The only thing more strongly forbidden by our culture is eating people (even if they are already dead). We enjoy eating members of other species, however. Many of us shrink from judicial execution of even the most horrible human criminals, while we cheerfully countenance the shooting without trial of fairly mild animal pests. Indeed we kill members of other harmless species as a means of recreation and amusement. A human foetus, with no more human feeling than an amoeba, enjoys a reverence and legal protection far in excess of those granted to an adult chimpanzee. Yet the chimp feels and thinks, and according to recent experimental evidence-may even be capable of learning a form of human language. The foetus belongs to our own species, and is instantly accorded special privileges and rights because of it. Whether the ethic of 'speciesism', to use Richard Ryder's term, can be put on a logical footing any more sound than that of 'racism', I do not know. What I do know is that it has no proper basis in evolutionary biology.

The muddle in human ethics over the level at which altruism is desirable-family, nation, race, species, or all living tilings-is mirrored by a parallel muddle in biology over the level at which altruism is to be expected according to the theory of evolution. Even the group-selectionist would not be surprised to find members of rival groups being nasty to each other: in this way, like trade unionists or soldiers, they are favouring their own group in the struggle for limited resources. But then it is worth asking how the group-selectionist decides which level is the important one. If selection goes on between groups within a species, and between species, why should it not also go on between larger groupings?

Species are grouped together into genera, genera into orders, and orders into classes. Lions and antelopes are both members of the class Mammalia, as are we. Should we then not expect lions to refrain from killing antelopes, 'for the good of the mammals'? Surely they should hunt birds or reptiles instead, in order to prevent the extinction of the class.

But then, what of the need to perpetuate the whole phylum of vertebrates?

T H E R E P L I C A T O R S

Haemoglobin is a modern molecule, used to illustrate the principle that atoms tend to fall into stable patterns. The point that is relevant here is that, before the coming of life on earth, some rudimentary evolution of molecules could have occurred by ordinary processes of physics and chemistry. There is no need to think of design or purpose or directedness.

If a group of atoms in the presence of energy falls into a stable pattern it will tend to stay that way. The earliest form of natural selection was

simply a selection of stable forms and a rejection of unstable ones. There is no mystery about this. It had to happen by definition.

Processes analogous to these must have given rise to the 'primeval soup' which biologists and chemists believe constituted the seas some three to four thousand million years ago. The organic substances became locally concentrated, perhaps in drying scum round the shores, or in tiny suspended droplets. Under the further influence of energy such as ultraviolet light from the sun, they combined into larger molecules.

Nowadays large organic molecules would not last long enough to be noticed: they would be quickly absorbed and broken down by bacteria or other living creatures. But bacteria and the rest of us are late-comers, and in those days large organic molecules could drift unmolested through the thickening broth.

At some point a particularly remarkable molecule was formed by accident. We will call it the Replicator. It may not necessarily have been the biggest or the most complex molecule around, but it had the extraordinary property of being able to create copies of itself This may seem a very unlikely sort of accident to happen. So it was. It was exceedingly improbable. In the lifetime of a man, things that are that improbable can be treated for practical purposes as impossible. That is why you will never win a big prize on the football pools. But in our human estimates of what is probable and what is not, we are not used to dealing in hundreds of millions of years. If you filled in pools coupons every week for a hundred million years you would very likely win several jackpots.

Actually a molecule that makes copies of itself is not as difficult to imagine as it seems at first, and it only had to arise once. Think of the replicator as a mould or template. Imagine it as a large molecule consisting of a complex chain of various sorts of building block molecules. The small building blocks were abundantly available in the soup surrounding the replicator. Now suppose that each building block has an affinity for its own kind. Then whenever a building block from out in the soup lands up next to a part of the replicator for which it has an affinity, it will tend to stick there. The building blocks that attach themselves in this way will automatically be arranged in a sequence that mimics that of the replicator itself. It is easy then to think of them joining up to form a stable chain just as in the formation of the original replicator. This process could continue as a progressive stacking up, layer upon layer. This is how crystals are formed. On the other hand, the two chains might split apart, in which case we have two replicators, each of which can go on to make further copies.

So we seem to arrive at a large population of identical replicas. But now we must mention an important property of any copying process: it is not perfect. Mistakes will happen. I hope there are no misprints in this blog, but if you look carefully you may find one or two. They will probably not seriously distort the meaning of the sentences, because they will be 'first generation' errors. But imagine the days before printing, when books such as the Gospels were copied by hand. All scribes, however careful, are bound to make a few errors, and some are not above a little wilful 'improvement'. If they all copied from a single master original, meaning would not be greatly perverted. But let copies be made from other copies, which in their turn were made from other copies, and errors will start to become cumulative and serious. We tend to regard erratic copying as a bad thing, and in the case of human documents it is hard to think of examples where errors can be described as improvements. I suppose the scholars of the Septuagint could at least be said to have started something big when they mistranslated the Hebrew word for 'young woman' into the Greek word for 'virgin', coming up with the prophecy: 'Behold a virgin shall conceive and bear a son .. .' Anyway, as we shall see, erratic copying in biological replicators can in a real sense give rise to improvement, and it was essential for the progressive evolution of life that some errors were made. We do not know how accurately the original replicator molecules made their copies. Their modem descendants, the DNA molecules, are astonishingly faithful compared with the most high fidelity human copying process, but even they occasionally make mistakes, and it is ultimately these mistakes that make evolution possible. Probably the original replicators were far more erratic, but in any case we may be sure that mistakes were made, and these mistakes were cumulative.

As mis-copyings were made and propagated, the primeval soup became filled by a population not of identical replicas, but of several varieties of replicating molecules, all 'descended' from the same ancestor. Would some varieties have been more numerous than others? Almost certainly yes. Some varieties would have been inherently more stable than others. Certain molecules, once formed, would be less likely than others to break up again. These types would become relatively numerous in the soup, not only as a direct logical consequence of their 'longevity', but also because they would have a long time available for making copies of themselves. Replicators of high longevity would therefore tend to become more numerous and, other things being equal, there would have been an 'evolutionary trend' towards greater longevity in the population of molecules.

But other things were probably not equal, and another property of a replicator variety that must have had even more importance in spreading it through the population was speed of replication or 'fecundity'. If replicator molecules of type A make copies of themselves on average once a week while those of type B make copies of themselves once an hour, it is not difficult to see that pretty soon type A molecules are going to be far outnumbered, even if they 'live' much longer than B molecules. There would therefore probably have been an 'evolutionary trend' towards higher 'fecundity' of molecules in the soup. A third characteristic of replicator molecules which would have been positively selected is accuracy of replication. If molecules of type X and type Y last the same length of time and replicate at the same rate, but X makes a mistake on average every tenth replication while Y makes a mistake only every hundredth replication, Y will obviously become more numerous. The X contingent in the population loses not only the errant 'children' themselves, but also all their descendants, actual or potential. If you already know something about evolution, you may find something slightly paradoxical about the last point. Can we reconcile the idea that copying errors are an essential prerequisite for evolution to occur, with the statement that natural selection favours high copying-fidelity? The answer is that although evolution may seem, in some vague sense, a 'good thing', especially since we are the product of it, nothing actually 'wants' to evolve. Evolution is something that happens, willy-nilly, in spite of all the efforts of the replicators (and nowadays of the genes) to prevent it from happening.

The next important link in the argument, one that Darwin himself laid stress on (although he was talking about animals and plants, not molecules) is competition. The primeval soup was not capable of supporting an infinite number of replicator molecules. For one thing, the earth's size is finite, but other limiting factors must also have been important. In our picture of the replicator acting as a template or mould, we supposed it to be bathed in a soup rich in the small building block molecules necessary to make copies. But when the replicators became numerous, building blocks must have been used up at such a rate that they became a scarce and precious resource. Different varieties or strains of replicator must have competed for them. We have considered the factors that would have increased the numbers of favoured kinds of replicator. We can now see that less-favoured varieties must actually have become less numerous because of competition, and ultimately many of their lines must have gone extinct. There was a struggle for existence among replicator varieties. They did not know they were struggling, or worry about it; the struggle was conducted without any hard feelings, indeed without feelings of any kind. But they were struggling, in the sense that any mis-copying that resulted in a new higher level of stability, or a new way of reducing the stability of rivals, was automatically preserved and multiplied. The process of improvement was cumulative. Ways of increasing stability and of decreasing rivals' stability became more elaborate and more efficient. Some of them may even have 'discovered' how to break up molecules of rival varieties chemically, and to use the building blocks so released for making their own copies. These proto-carnivores simultaneously obtained food and removed competing rivals. Other replicators perhaps discovered how to protect themselves, either chemically, or by building a physical wall of protein around themselves. This may have been how the first living cells appeared. Replicators began not merely to exist, but to construct for themselves containers, vehicles for their continued existence. The replicators that survived were the ones that built survival machines for themselves to live in. The first survival machines probably consisted of nothing more than a protective coat. But making a living got steadily harder as new rivals arose with better and more effective survival machines. Survival machines got bigger and more elaborate, and the process was cumulative and progressive.

Was there to be any end to the gradual improvement in the techniques and artifices used by the replicators to ensure their own continuation in the world? There would be plenty of time for improvement. What weird engines of self-preservation would the millennia bring forth? Four thousand million years on, what was to be the fate of the ancient replicators? They did not die out, for they are past masters of the survival arts. But do not look for them floating loose in the sea; they gave up that cavalier freedom long ago. Now they swarm in huge colonies, safe inside gigantic lumbering robots, sealed off from the outside world, communicating with it by tortuous indirect routes, manipulating it by remote control. They are in you and in me; they created us, body and mind; and their preservation is the ultimate rationale for our existence. They have come a long way, those replicators. Now they go by the name of genes, and we are their survival machines.

I M M O R T A L C O I L S

A DNA molecule is a long chain of building blocks, small molecules called nucleotides. Just as protein molecules are chains of amino acids, so DNA molecules are chains of nucleotides. A DNA molecule is too small to be seen, but its exact shape has been ingeniously worked out by indirect means. It consists of a pair of nucleotide chains twisted together in an elegant spiral; the 'double helix'; the 'immortal coil'. The nucleotide building blocks come in only four different kinds, whose names may be shortened to A, T, C, and G. These are the same in all animals and plants. What differs is the order in which they are strung together. A G building block from a man is identical in every particular to a G building block from a snail. But the sequence of building blocks in a man is not only different from that in a snail. It is also different-though less so-from the sequence in every other man (except in the special case of identical twins).

Our DNA lives inside our bodies. It is not concentrated in a particular part of the body, but is distributed among the cells. There are about a thousand million million cells making up an average human body, and, with some exceptions which we can ignore, every one of those cells contains a complete copy of that body's DNA. This DNA can be regarded as a set of instructions for how to make a body, written in the A, T, C, G alphabet of the nucleotides. It is as though, in every room of a gigantic building, there was a book-case containing the architect's plans for the entire building. The 'book-case' in a cell is called the nucleus. The architect's plans run to 46 volumes in man-the number is different in other species. The 'volumes' are called chromosomes. They are visible under a microscope as long threads, and the genes are strung out along them in order. It is not easy, indeed it may not even be meaningful, to decide where one gene ends and the next one begins. Fortunately, this does not matter for our purposes.

The evolutionary importance of the fact that genes control embryonic development is this: it means that genes are at least partly responsible for their own survival in the future, because their survival depends on the efficiency of the bodies in which they live and which they helped to build. Once upon a time, natural selection consisted of the differential survival of replicators floating free in the primeval soup. Now, natural selection favours replicators that are good at building survival machines, genes that are skilled in the art of controlling embryonic development. In this, the replicators are no more conscious or purposeful than they ever were. The same old processes of automatic selection between rival molecules by reason of their longevity, fecundity, and copying-fidelity, still go on as blindly and as inevitably as they did in the far-off days. Genes have no foresight. They do not plan ahead. Genes just are, some genes more so than others, and that is all there is to it. But the qualities that determine a gene's longevity and fecundity are not so simple as they were. Not by a long way.

I said that the plans for building a human body are spelt out in 46 volumes. In fact this was an over-simplification. The truth is rather bizarre. The 46 chromosomes consist of 23 pairs of chromosomes. We might say that, filed away in the nucleus of every cell, are two alternative sets of 23 volumes of plans. Call them Volume 1a and 1b, Volume 2a and Volume 2b etc., down to Volume 23a and Volume 23b. Of course the identifying numbers I use for volumes and, later, pages, are purely arbitrary.

We receive each chromosome intact from one of our two parents, in whose testis or ovary it was assembled. Volumes 1a, 2a, 3a, ... came, say, from the father. Volumes 1b, 2b, 3b,... came from the mother. It is very difficult in practice, but in theory you could look with a microscope at the 46 chromosomes in any one of your cells, and pick out the 23 that came from your father and the 23 that came from your mother.

The paired chromosomes do not spend all their lives physically in contact with each other, or even near each other. In what sense then are they 'paired'? In the sense that each volume coming originally from the father can be regarded, page for page, as a direct alternative to one particular volume coming originally from the mother. For instance, Page 6 of Volume 13a and Page 6 of Volume 13b might both be 'about' eye colour; perhaps one says 'blue' while the other says 'brown'.

Meiosis occurs only in the production of the sex cells; the sperms or eggs. Sperms and eggs are unique among our cells in that, instead of containing 46 chromosomes, they contain only 23. This is, of course, exactly half of 46-convenient when they fuse in sexual fertilization to make a new individual! Meiosis is a special kind of cell division, taking place only in testicles and ovaries, in which a cell with the full double set of 46 chromosomes divides to form sex cells with the single set of 23.

A sperm, with its 23 chromosomes, is made by the meiotic division of one of the ordinary 46-chromosome cells in the testicle. Which 23 are put into any given sperm cell? It is clearly important that a sperm should not get just any old 23 chromosomes: it mustn't end up with two copies of Volume 13 and none of Volume 17. It would theoretically be possible for an individual to endow one of his sperms with chromosomes which came, say, entirely from his mother; that is Volume 1b, 2b, 3b,..., 23b. In this unlikely event, a child conceived by the sperm would inherit half her genes from her paternal grandmother, and none from her paternal grandfather. But in fact this kind of gross, whole-chromosome distribution does not happen. The truth is rather more complex. Remember that the volumes (chromosomes) are to be thought of as looseleaf binders. What happens is that, during the manufacture of the sperm, single pages, or rather multi-page chunks, are detached and swapped with the corresponding chunks from the alternative volume. So, one particular sperm cell might make up its Volume 1 by taking the first 65 pages from Volume 1a, and pages 66 to the end from Volume 1b. This sperm cell's other 22 volumes would be made up in a similar way.

Therefore every sperm cell made by an individual is unique, even though all his sperms assembled their 23 chromosomes from bits of the same set of 46 chromosomes. Eggs are made in a similar way in ovaries, and they too are all unique.

The gene complex is just a long string of nucleotide letters, not divided into discrete pages in an obvious way at all. To be sure, there are special symbols for END OF PROTEIN CHAIN MESSAGE and START OF PROTEIN CHAIN MESSAGE written in the same four-letter alphabet as the protein messages themselves. In between these two punctuation marks are the coded instructions for making one protein. If we wish, we can define a single gene as a sequence of nucleotide letters lying between a start and an end symbol, and coding for one protein chain. The word cistron has been used for a unit defined in this way, and some people use the word gene interchangeably with cistron. But crossing-over does not respect boundaries between cistrons. Splits may occur within cistrons as well as between them. It is as though the architect's plans were written out, not on discrete pages, but on 46 rolls of ticker tape. Cistrons are not of fixed length. The only way to tell where one cistron ends and the next begins would be to read the symbols on the tape, looking for end of message and start of message symbols. Crossing-over is represented by taking matching paternal and maternal tapes, and cutting and exchanging matching portions, regardless of what is written on them.

A gene is defined as any portion of chromosomal material that potentially lasts for enough generations to serve as a unit of natural selection - a replicator with high copying-fidelity.

The shorter a genetic unit is, the longer in generations-it is likely to live. In particular, the less likely it is to be split by any one crossing-over.

The average life-expectancy of a genetic unit can conveniently be expressed in generations, which can in turn be translated into years. If we take a whole chromosome as our presumptive genetic unit, its life story lasts for only one generation. Suppose it is your chromosome number 8a, inherited from your father. It was created inside one of your father's testicles, shortly before you were conceived. It had never existed before in the whole history of the world. It was created by the meiotic shuffling process, forged by the coming together of pieces of chromosome from your paternal grandmother and your paternal grandfather. It was placed inside one particular sperm, and it was unique. The sperm was one of several millions, a vast armada of tiny vessels, and together they sailed into your mother. This particular sperm (unless you are a nonidentical twin) was the only one of the flotilla which found harbour in one of your mother's eggs-that is why you exist. The genetic unit we are considering, your chromosome number 8a, set about replicating itself along with all the rest of your genetic material. Now it exists, in duplicate form, all over your body. But when you in your turn come to have children, this chromosome will be destroyed when you manufacture eggs (or sperms). Bits of it will be interchanged with bits of your maternal chromosome number 8b. In any one sex cell, a new chromosome number 8 will be created, perhaps 'better' than the old one, perhaps 'worse', but, barring a rather improbable coincidence, definitely different, definitely unique. The life-span of a chromosome is one generation.

One of the neatest examples of inversion concerns the phenomenon known as mimicry. Some butterflies taste nasty. They are usually brightly and distinctively coloured, and birds learn to avoid them by their 'warning' marks. Now other species of butterfly that do not taste nasty cash in. They mimic the nasty ones. They are born looking like them in colour and shape (but not taste). They frequently fool human naturalists, and they also fool birds. A bird who has once tasted a genuinely nasty butterfly tends to avoid all butterflies that look the same. This includes the mimics, and so genes for mimicry are favoured by natural selection. That is how mimicry evolves. There are many different species of 'nasty' butterfly and they do not all look alike. A mimic cannot resemble all of them: it has to commit itself to one particular nasty species. In general, any particular species of mimic is a specialist at mimicking one particular nasty species. But there are species of mimic that do something very strange. Some individuals of the species mimic one nasty species; other individuals mimic another. Any individual who was intermediate or who tried to mimic both would soon be eaten; but such intermediates are not born. Just as an individual is either definitely male or definitely female, so an individual butterfly mimics either one nasty species or the other. One butterfly may mimic species A while his brother mimics species B.

Another aspect of the particulateness of the gene is that it does not grow senile; it is no more likely to die when it is a million years old than when it is only a hundred. It leaps from body to body down the generations, manipulating body after body in its own way and for its own ends, abandoning a succession of mortal bodies before they sink in senility and death. The genes are the immortals, or rather, they are defined as genetic entities that come close to deserving the title. We, the individual survival machines in the world, can expect to live a few more decades. But the genes in the world have an expectation of life that must be measured not in decades but in thousands and millions of years.

In sexually reproducing species, the individual is too large and too temporary a genetic unit to qualify as a significant unit of natural selection. The group of individuals is an even larger unit. Genetically speaking, individuals and groups are like clouds in the sky or duststorms in the desert. They are temporary aggregations or federations. They are not stable through evolutionary time. Populations may last a long while, but they are constantly blending with other populations and so losing their identity. They are also subject to evolutionary change from within. A population is not a discrete enough entity to be a unit of natural selection, not stable and unitary enough to be 'selected' in preference to another population.

An individual body seems discrete enough while it lasts, but alas, how long is that? Each individual is unique. You cannot get evolution by selecting between entities when there is only one copy of each entity! Sexual reproduction is not replication. Just as a population is contaminated by other populations, so an individual's posterity is contaminated by that of his sexual partner. Your children are only half you, your grandchildren only a quarter you. In a few generations the most you can hope for is a large number of descendants, each of whom bears only a tiny portion of you-a few genes-even if a few do bear your surname as well. Individuals are not stable things, they are fleeting. Chromosomes too are shuffled into oblivion, like hands of cards soon after they are dealt. But the cards themselves survive the shuffling. The cards are the genes. The genes are not destroyed by crossing-over, they merely change partners and march on. Of course they march on. That is their business. They are the replicators and we are their survival machines. When we have served our purpose we are cast aside. But genes are denizens of geological time: genes are forever.

The question of why we die of old age is a complex one, and the details are beyond the scope of this book. In addition to particular reasons, some more general ones have been proposed. For example, one theory is that senility represents an accumulation of deleterious copying errors and other kinds of gene damage which occur during the individual's lifetime. Another theory, due to Sir Peter Medawar, is a good example of evolutionary thinking in terms of gene selection. Medawar first dismisses traditional arguments such as: 'Old individuals die as an act of altruism to the rest of the species, because if they stayed around when they were too decrepit to reproduce, they would clutter up the world to no good purpose.' As Medawar points out, this is a circular argument, assuming what it sets out to prove, namely that old animals are too decrepit to reproduce. It is also a naive group-selection or species-selection kind of explanation, although that part of it could be rephrased more respectably. Medawar's own theory has a beautiful logic.

Senile decay is simply a byproduct of the accumulation in the gene pool of late-acting lethal and semi-lethal genes, which have been allowed to slip through the net of natural selection simply because they are late-acting.

The aspect that Medawar himself emphasizes is that selection will favour genes that have the effect of postponing the operation of other, lethal genes, and it will also favour genes that have the effect of hastening the effect of good genes. It may be that a great deal of evolution consists of genetically-controlled changes in the time of onset of gene activity.

As an aside, one of the good features of this theory is that it leads us to some rather interesting speculations. For instance it follows from it that if we wanted to increase the human life span, there are two general ways in which we could do it. Firstly, we could ban reproduction before a certain age, say forty. After some centuries of this the minimum age limit would be raised to fifty, and so on. It is conceivable that human longevity could be pushed up to several centuries by this means. I cannot imagine that anyone would seriously want to institute such a policy.

Secondly we could try to 'fool' genes into thinking that the body they are sitting in is younger than it really is. In practice this would mean identifying changes in the internal chemical environment of a body that take place during ageing. Any of these could be the 'cues' that 'turn on' late-acting lethal genes. By simulating the superficial chemical properties of a young body it might be possible to prevent the turning on of lateacting deleterious genes. The interesting point is that chemical signals of old age need not in any normal sense be deleterious in themselves. For instance, suppose that it incidentally happens to be a fact that a substance S is more concentrated in the bodies of old individuals than of young individuals. S in itself might be quite harmless, perhaps some substance in the food which accumulates in the body over time. But automatically, any gene that just happened to exert a deleterious effect in the presence of S, but which otherwise had a good effect, would be positively selected in the gene pool, and would in effect be a gene 'for' dying of old age. The cure would simply be to remove S from the body. What is revolutionary about this idea is that S itself is only a 'label' for old age. Any doctor who noticed that high concentrations of S tended to lead to death, would probably think of S as a kind of poison, and would rack his brains to find a direct causal link between S and bodily malfunctioning. But in the case of our hypothetical example, he might be wasting his time! There might also be a substance Y a 'label' for youth in the sense that it was more concentrated in young bodies than in old ones. Once again, genes might be selected that would have good effects in the presence of Y but which would be deleterious in its absence. Without having any way of knowing what S or Y are-there could be many such substances-we can simply make the general prediction that the more you can simulate or mimic the properties of a young body in an old one, however superficial these properties may seem, the longer should that old body live.

Crossing-over does not always have to happen. Male fruit-flies do not do it. There is a gene that has the effect of suppressing crossing-over in females as well. If we were to breed a population of flies in which this gene was universal, the chromosome in a 'chromosome pool' would become the basic indivisible unit of natural selection. In fact, if we followed our definition to its logical conclusion, a whole chromosome would have to be regarded as one 'gene'.

Then again, alternatives to sex do exist. Female greenflies can bear live, fatherless, female offspring, each one containing all the genes of its mother. (Incidentally, an embryo in her mother's 'womb' may have an even smaller embryo inside her own womb. So a greenfly female may give birth to a daughter and a grand-daughter simultaneously, both of them being equivalent to her own identical twins.) Many plants propagate vegetatively by sending out suckers. In this case we might prefer to speak of growth rather than of reproduction; but then, if you think about it, there is rather little distinction between growth and non-sexual reproduction anyway, since both occur by simple mitotic cell division. Sometimes the plants produced by vegetative reproduction become detached from the 'parent'. In other cases, for instance elm trees, the connecting suckers remain intact. In fact an entire elm wood might be regarded as a single individual. So, the question is: if greenflies and elm trees don't do it, why do the rest of us go to such lengths to mix our genes up with somebody else's before we make a baby? It does seem an odd way to proceed. Why did sex, that bizarre perversion of straightforward replication, ever arise in the first place? What is the good of sex?

This is an extremely difficult question for the evolutionist to answer. Most serious attempts to answer it involve sophisticated mathematical reasoning. I am frankly going to evade it except to say one thing. This is that at least some of the difficulty that theorists have with explaining the evolution of sex results from the fact that they habitually think of the individual as trying to maximize the number of his genes that survive. In these terms, sex appears paradoxical because it is an 'inefficient' way for an individual to propagate her genes: each child has only 50 per cent of the individual's genes, the other 50 per cent being provided by the sexual partner. If only, like a greenfly, she would bud-off children who were exact replicas of herself, she would pass 100 per cent of her genes on to the next generation in the body of every child. This apparent paradox has driven some theorists to embrace group-selectionism, since it is relatively easy to think of group-level advantages for sex. As W. F. Bodmer has succinctly put it, sex 'facilitates the accumulation in a single individual of advantageous mutations which arose separately in different individuals.'

But the paradox seems less paradoxical if we follow the argument of this book, and treat the individual as a survival machine built by a shortlived confederation of long-lived genes. 'Efficiency' from the whole individual's point of view is then seen to be irrelevant. Sexuality versus non-sexuality will be regarded as an attribute under single-gene control, just like blue eyes versus brown eyes. A gene 'for' sexuality manipulates all the other genes for its own selfish ends. So does a gene for crossingover. There are even genes-called mutators-that manipulate the rates of copying-errors in other genes. By definition, a copying error is to the disadvantage of the gene which is miscopied. But if it is to the advantage of the selfish mutator gene that induces it, the mutator can spread through the gene pool. Similarly, if crossing-over benefits a gene for crossing-over, that is a sufficient explanation for the existence of crossing-over. And if sexual, as opposed to non-sexual, reproduction benefits a gene for sexual reproduction, that is a sufficient explanation for the existence of sexual reproduction. Whether or not it benefits all the rest of an individual's genes is comparatively irrelevant. Seen from the selfish gene's point of view, sex is not so bizarre after all.

Sex is not the only apparent paradox that becomes less puzzling the moment we learn to think in selfish gene terms. For instance, it appears that the amount of DNA in organisms is more than is strictly necessary for building them: a large fraction of the DNA is never translated into protein. From the point of view of the individual organism this seems paradoxical. If the 'purpose' of DNA is to supervise the building of bodies, it is surprising to find a large quantity of DNA which does no such thing. Biologists are racking their brains trying to think what useful task this apparently surplus DNA is doing. But from the point of view of the selfish genes themselves, there is no paradox. The true 'purpose' of DNA is to survive, no more and no less. The simplest way to explain the surplus DNA is to suppose that it is a parasite, or at best a harmless but useless passenger, hitching a ride in the survival machines created by the other DNA.

T H E G E N E M A C H I N E

Survival machines began as passive receptacles for the genes, providing little more than walls to protect them from the chemical warfare of their rivals and the ravages of accidental molecular bombardment. In the early days they 'fed' on organic molecules freely available in the soup. This easy life came to an end when the organic food in the soup, which had been slowly built up under the energetic influence of centuries of sunlight, was all used up. A major branch of survival machines, now called plants, started to use sunlight directly themselves to build up complex molecules from simple ones, re-enacting at much higher speed the synthetic processes of the original soup. Another branch, now known as animals, 'discovered' how to exploit the chemical labours of the plants, either by eating them, or by eating other animals. Both main branches of survival machines evolved more and more ingenious tricks to increase their efficiency in their various ways of life, and new ways of life were continually being opened up. Sub-branches and sub-sub-branches evolved, each one excelling in a particular specialized way of making a living: in the sea, on the ground, in the air, underground, up trees, inside other living bodies. This sub-branching has given rise to the immense diversity of animals and plants which so impresses us today.

There may have been a time when sense organs communicated more or less directly with muscles; indeed, sea anemones are not far from this state today, since for their way of life it is efficient. But to achieve more complex and indirect relationships between the timing of events in the outside world and the timing of muscular contractions, some kind of brain was needed as an intermediary. A notable advance was the evolutionary 'invention' of memory. By this device, the timing of muscle contractions could be influenced not only by events in the immediate past, but by events in the distant past as well. The memory, or store, is an essential part of a digital computer too. Computer memories are more reliable than human ones, but they are less capacious, and enormously less sophisticated in their techniques of information-retrieval.

The genes too control the behaviour of their survival machines, not directly with their fingers on puppet strings, but indirectly like the computer programmer. All they can do is to set it up beforehand; then the survival machine is on its own, and the genes can only sit passively inside. Why are they so passive? Why don't they grab the reins and take charge from moment to moment? The answer is that they cannot because of time-lag problems. This is best shown by another analogy, taken from science fiction. A for Andromeda by Fred Hoyle and John Elliot is an exciting story, and, like all good science fiction, it has some interesting scientific points lying behind it. Strangely, the book seems to lack explicit mention of the most important of these underlying points. It is left to the reader's imagination. I hope the authors will not mind if I spell it out here.

There is a civilization 200 light-years away, in the constellation of Andromeda. They want to spread their culture to distant worlds. How best to do it? Direct travel is out of the question. The speed of light imposes a theoretical upper limit to the rate at which you can get from one place to another in the universe, and mechanical considerations impose a much lower limit in practice. Besides, there may not be all that many worlds worth going to, and how do you know which direction to go in? Radio is a better way of communicating with the rest of the universe, since, if you have enough power to broadcast your signals in all directions rather than beam them in one direction, you can reach a very large number of worlds (the number increasing as the square of the distance the signal travels). Radio waves travel at the speed of light, which means the signal takes 200 years to reach earth from Andromeda.

The trouble with this sort of distance is that you can never hold a conversation. Even if you discount the fact that each successive message from earth would be transmitted by people separated from each other by twelve generations, it would be just plain wasteful to attempt to converse over such distances.

This problem will soon arise in earnest for us: it takes about four minutes for radio waves to travel between earth and Mars. There can be no doubt that spacemen will have to get out of the habit of conversing in short alternating sentences, and will have to use long soliloquies or monologues, more like letters than conversations. As another example, Roger Payne has pointed out that the acoustics of the sea have certain peculiar properties, which mean that the exceedingly loud 'song' of some whales could theoretically be heard all the way round the world, provided the whales swim at a certain depth. It is not known whether they actually do communicate with each other over very great distances, but if they do they must be in much the same predicament as an astronaut on Mars. The speed of sound in water is such that it would take nearly two hours for the song to travel across the Atlantic Ocean and for a reply to return. I suggest this as an explanation for the fact that some whales deliver a continuous soliloquy, without repeating themselves, for a full eight minutes. They then go back to the beginning of the song and repeat it all over again, many times over, each complete cycle lasting about eight minutes.

The Andromedans of the story did the same thing. Since there was no point in waiting for a reply, they assembled everything they wanted to say into one huge unbroken message, and then they broadcast it out into space, over and over again, with a cycle time of several months. Their message was very different from that of the whales, however. It consisted of coded instructions for the building and programming of a giant computer. Of course the instructions were in no human language, but almost any code can be broken by a skilled cryptographer, especially if the designers of the code intended it to be easily broken. Picked up by the Jodrell Bank radio telescope, the message was eventually decoded, the computer built, and the program run. The results were nearly disastrous for mankind, for the intentions of the Andromedans were not universally altruistic, and the computer was well on the way to dictatorship over the world before the hero eventually finished it off with an axe.

From our point of view, the interesting question is in what sense the Andromedans could be said to be manipulating events on Earth. They had no direct control over what the computer did from moment to moment; indeed they had no possible way of even knowing the computer had been built, since the information would have taken 200 years to get back to them. The decisions and actions of the computer were entirely its own. It could not even refer back to its masters for general policy instructions. All its instructions had to be built-in in advance, because of the inviolable 200 year barrier. In principle, it must have been programmed very much like a chess-playing computer, but with greater flexibility and capacity for absorbing local information. This was because the program had to be designed to work not just on earth, but on any world possessing an advanced technology, any of a set of worlds whose detailed conditions the Andromedans had no way of knowing. Just as the Andromedans had to have a computer on earth to take day-to-day decisions for them, our genes have to build a brain. But the genes are not only the Andromedans who sent the coded instructions; they are also the instructions themselves. The reason why they cannot manipulate our puppet strings directly is the same: time-lags. Genes work by controlling protein synthesis. This is a powerful way of manipulating the world, but it is slow. It takes months of patiently pulling protein strings to build an embryo. The whole point about behaviour, on the other hand, is that it is fast. It works on a time-scale not of months but of seconds and fractions of seconds. Something happens in the world, an owl flashes overhead, a rustle in the long grass betrays prey, and in milliseconds nervous systems crackle into action, muscles leap, and someone's life is saved-or lost. Genes don't have reaction-times like that. Like the Andromedans, the genes can only do their best in advance by building a fast executive computer for themselves, and programming it in advance with rules and 'advice' to cope with as many eventualities as they can 'anticipate'. But life, like the game of chess, offers too many different possible eventualities for all of them to be anticipated. Like the chess programmer, the genes have to 'instruct' their survival machines not in specifics, but in the general strategies and tricks of the living trade.

One way for genes to solve the problem of making predictions in rather unpredictable environments is to build in a capacity for learning. Here the program may take the form of the following instructions to the survival machine: 'Here is a list of things defined as rewarding: sweet taste in the mouth, orgasm, mild temperature, smiling child. And here is a list of nasty things: various sorts of pain, nausea, empty stomach, screaming child. If you should happen to do something that is followed by one of the nasty things, don't do it again, but on the other hand repeat anything that is followed by one of the nice things.' The advantage of this sort of programming is that it greatly cuts down the number of detailed rules that have to be built into the original program; and it is also capable of coping with changes in the environment that could not have been predicted in detail. On the other hand, certain predictions have to be made still. In our example the genes are predicting that sweet taste in the mouth, and orgasm, are going to be 'good' in the sense that eating sugar and copulating are likely to be beneficial to gene survival. The possibilities of saccharine and masturbation are not anticipated according to this example; nor are the dangers of over-eating sugar in our environment where it exists in unnatural plenty.

Perhaps consciousness arises when the brain's simulation of the world becomes so complete that it must include a model of itself.

Whatever the philosophical problems raised by consciousness, for the purpose of this story it can be thought of as the culmination of an evolutionary trend towards the emancipation of survival machines as executive decision-takers from their ultimate masters, the genes. Not only are brains in charge of the day-to-day running of survival-machine affairs, they have also acquired the ability to predict the future and act accordingly. They even have the power to rebel against the dictates of the genes, for instance in refusing to have as many children as they are able to. But in this respect man is a very special case.

A G G R E S S I O N: S T A B I L I T Y A N D T H E S E L F I S H

M A C H I N E

An evolutionarily stable strategy or ESS is defined as a strategy which, if most members of a population adopt it, cannot be bettered by an alternative strategy. It is a subtle and important idea. Another way of putting it is to say that the best strategy for an individual depends on what the majority of the population are doing. Since the rest of the population consists of individuals, each one trying to maximize his own success, the only strategy that persists will be one which, once evolved, cannot be bettered by any deviant individual. Following a major environmental change there may be a brief period of evolutionary instability, perhaps even oscillation in the population. But once an ESS is achieved it will stay: selection will penalize deviation from it.

To apply this idea to aggression, consider one of Maynard Smith's simplest hypothetical cases. Suppose that there are only two sorts of fighting strategy in a population of a particular species, named hawk and dove. (The names refer to conventional human usage and have no connection with the habits of the birds from whom the names are derived: doves are in fact rather aggressive birds.) Any individual of our hypothetical population is classified as a hawk or a dove. Hawks always fight as hard and as unrestrainedly as they can, retreating only when seriously injured. Doves merely threaten in a dignified conventional way, never hurting anybody. If a hawk fights a dove the dove quickly runs away, and so does not get hurt. If a hawk fights a hawk they go on until one of them is seriously injured or dead. If a dove meets a dove nobody gets hurt; they go on posturing at each other for a long time until one of them tires or decides not to bother any more, and therefore backs down. For the time being, we assume that there is no way in which an individual can tell, in advance, whether a particular rival is a hawk or a dove. He only discovers this by fighting him, and he has no memory of past fights with particular individuals to guide him.

Now as a purely arbitrary convention we allot contestants 'points'. Say 50 points for a win, 0 for losing, -100 for being seriously injured, and -10 for

wasting time over a long contest. These points can be thought of as being directly convertible into the currency of gene survival. An individual who scores high points, who has a high average 'pay-off, is an individual who leaves many genes behind him in the gene pool. Within broad limits the actual numerical values do not matter for the analysis, but they help us to think about the problem.

The important thing is that we are not interested in whether hawks will tend to beat doves when they fight them. We already know the answer to that: hawks will always win. We want to know whether either hawk or dove is an evolutionarily stable strategy. If one of them is an ESS and the other is not, we must expect that the one which is the ESS will evolve. It is theoretically possible for there to be two ESSs. This would be true if, whatever the majority strategy of the population happened to be, whether hawk or dove, the best strategy for any given individual was to follow suit. In this case the population would tend to stick at whichever one of its two stable states it happened to reach first. However, as we shall now see, neither of these two strategies, hawk or dove, would in fact be evolutionarily stable on its own, and we should therefore not expect either of them to evolve. To show this we must calculate average pay-offs. Suppose we have a population consisting entirely of doves. Whenever they fight, nobody gets hurt. The contests consist of prolonged ritual tournaments, staring matches perhaps, which end only when one rival backs down. The winner then scores 50 points for gaining the resource in dispute, but he pays a penalty of -10 for wasting time over a long staring match, so scores 40 in all. The loser also is penalized -10 points for wasting time. On average, any one individual dove can expect to win half his contests and lose half. Therefore his average pay-off per contest is the average of +40 and - 10, which is +15. Therefore, every individual dove in a population of doves seems to be doing quite nicely. But now suppose a mutant hawk arises in the population. Since he is the only hawk around, every fight he has is against a dove. Hawks always beat doves, so he scores +50 every fight, and this is his average pay-off. He enjoys an enormous advantage over the doves, whose net pay-off is only +15. Hawk genes will rapidly spread through the population as a result. But now each hawk can no longer count on every rival he meets being a dove. To take an extreme example, if the hawk gene spread so successfully that the entire population came to consist of hawks, all fights would now be hawk fights. Things are now very different. When hawk meets hawk, one of them is seriously injured, scoring -100, while the winner scores +50. Each hawk in a population of hawks can expect to win half his fights and lose half his fights. His average expected pay-off per fight is therefore half-way between +50 and -100, which is -25. Now consider a single dove in a population of hawks. To be sure, he loses all his fights, but on the other hand he never gets hurt. His average pay-off is 0 in a population of hawks, whereas the average pay-off for a hawk in a population of hawks is -25. Dove genes will therefore tend to spread through the population. The way I have told the story it looks as if there will be a continuous oscillation in the population. Hawk genes will sweep to ascendancy; then, as a consequence of the hawk majority, dove genes will gain an advantage and increase in numbers until once again hawk genes start to prosper, and so on. However, it need not be an oscillation like this. There is a stable ratio of hawks to doves. For the particular arbitrary points system we are using, the stable ratio, if you work it out, turns out to be 5/12 doves to 7/12 hawks. When this stable ratio is reached, the average pay-off for hawks is exactly equal to the average pay-off for doves. Therefore selection does not favour either one of them over the other. If the number of hawks in the population started to drift upwards so that the ratio was no longer 7/12 doves would start to gain an extra advantage, and the ratio would swing back to the stable state. Just as we shall find the stable sex ratio to be 50:50, so the stable hawk to dove ratio in this hypothetical example is 7:5. In either case, if there are oscillations about the stable point, they need not be very large ones.

Superficially, this sounds a little like group selection, but it is really nothing of the kind. It sounds like group selection because it enables us to think of a population as having a stable equilibrium to which it tends to return when disturbed. But the ESS is a much more subtle concept than group selection. It has nothing to do with some groups being more successful than others. This can be nicely illustrated using the arbitrary points system of our hypothetical example. The average pay-off to an individual in a stable population consisting of 7/12 hawks and 5/12 doves, turns out to be 6 1/4. This is true whether the individual is a hawk or a dove. Now 6 1/4 is much less than the average pay-off for a dove in a population of doves (15). If only everybody would agree to be a dove, every single individual would benefit. By simple group selection, any group in which all individuals mutually agree to be doves would be far more successful than a rival group sitting at the ESS ratio. (As a matter of fact, a conspiracy of nothing but doves is not quite the most successful possible group. In a group consisting of 1/6 hawks and 5/6 doves, the average pay-off per contest is 16 2/3. This is the most successful possible conspiracy, but for present purposes we can ignore it. A simpler all-dove conspiracy, with its average pay-off for each individual of 15, is far better for every single individual than the ESS would be.) Group selection theory would therefore predict a tendency to evolve towards an all-dove conspiracy, since a group that contained a 7/12 proportion of hawks would be less successful. But the trouble with conspiracies, even those that are to everybody's advantage in the long run, is that they are open to abuse. It is true that everybody does better in an all-dove group than he would in an ESS group. But unfortunately, in conspiracies of doves, a single hawk does so extremely well that nothing could stop the evolution of hawks. The conspiracy is therefore bound to be broken by treachery from within. An ESS is stable, not because it is particularly good for the individuals participating in it, but simply because it is immune to treachery from within.

So far we have considered only what Maynard Smith calls 'symmetric' contests. This means we have assumed that the contestants are identical in all respects except their fighting strategy. Hawks and doves are assumed to be equally strong, to be equally well endowed with weapons and with armour, and to have an equal amount to gain from winning. This is a convenient assumption to make for a model, but it is not very realistic. Parker and Maynard Smith went on to consider asymmetric contests. For example, if individuals vary in size and fighting ability, and each individual is capable of gauging a rival's size in comparison to his own, does this affect the ESS that emerges? It most certainly does. There seem to be three main sorts of asymmetry. The first we have just met: individuals may differ in their size or fighting equipment. Secondly, individuals may differ in how much they have to gain from winning. For instance an old male, who has not long to live anyway, might have less to lose if he is injured than a young male with the bulk of his reproductive life ahead of him.

Thirdly, it is a strange consequence of the theory that a purely arbitrary, apparently irrelevant, asymmetry can give rise to an ESS, since it can be used to settle contests quickly. For instance it will usually be the case that one contestant happens to arrive at the location of the contest earlier than the other. Call them 'resident' and 'intruder' respectively. For the sake of argument, I am assuming that there is no general advantage attached to being a resident or an intruder. As we shall see, there are practical reasons why this assumption may not be true, but that is not the point. The point is that even if there were no general reason to suppose that residents have an advantage over intruders, an ESS depending on the asymmetry itself would be likely to evolve. A simple analogy is to humans who settle a dispute quickly and without fuss by tossing a coin. The conditional strategy: 'If you are the resident, attack; if you are the intruder, retreat', could be an ESS. Since the asymmetry is assumed to be arbitrary, the opposite strategy: 'If resident, retreat; if intruder, attack' could also be stable. Which of the two ESSs is adopted in a particular population would depend on which one happens to reach a majority first. Once a majority of individuals is playing one of these two conditional strategies, deviants from it are penalized. Hence, by definition, it is an ESS. For instance, suppose all individuals are playing 'resident wins, intruder runs away'. This means they will win half their fights and lose half their fights. They will never be injured and they will never waste time, since all disputes are instantly settled by arbitrary convention. Now consider a new mutant rebel. Suppose he plays a pure hawk strategy, always attacking and never retreating. He will win when his opponent is an intruder. When his opponent is a resident he will run a grave risk of injury. On average he will have a lower pay-off than individuals playing according to the arbitrary rules of the ESS. A rebel who tries the reverse convention 'if resident run away, if intruder attack', will do even worse. Not only will he frequently be injured, he will also seldom win a contest. Suppose, though, that by some chance events individuals playing this reverse convention managed to become the majority. In this case their strategy would then become the stable norm, and deviation from it would be penalized. Conceivably, if we watched a population for many generations we would see a series of occasional flips from one stable state to the other.

However, in real life, truly arbitrary asymmetries probably do not exist. For instance, residents probably tend to have a practical advantage over intruders. They have better knowledge of local terrain. An intruder is perhaps more likely to be out of breath because he moved into the battle area, whereas the resident was there all the time. There is a more abstract reason why, of the two stable states, the 'resident wins, intruder retreats', one is the more probable in nature. This is that the reverse strategy, 'intruder wins, resident retreats' has an inherent tendency to self-destruction-it is what Maynard Smith would call a paradoxical strategy. In any population sitting at this paradoxical ESS, individuals would always be striving never to be caught as residents: they would always be trying to be the intruder in any encounter. They could only achieve this by ceaseless, and otherwise pointless, moving around! Quite apart from the costs in time and energy that would be incurred, this evolutionary trend would, of itself, tend to lead to the category 'resident' ceasing to exist. In a population sitting at the other stable state, 'resident wins, intruder retreats', natural selection would favour individuals who strove to be residents. For each individual, this would mean holding on to a particular piece of ground, leaving it as little as possible, and appearing to 'defend' it. As is now well known, such behaviour is commonly observed in nature, and goes by the name of 'territorial defence'.

The neatest demonstration I know of this form of behavioural asymmetry was provided by the great ethologist Niko Tinbergen, in an experiment of characteristically ingenious simplicity. He had a fish-tank containing two male sticklebacks. The males had each built nests, at opposite ends of the tank, and each 'defended' the territory around his own nest. Tinbergen placed each of the two males in a large glass test-tube, and he held the two tubes next to each other and watched the males trying to fight each other through the glass. Now comes the interesting result. When he moved the two tubes into the vicinity of male A's nest, male A assumed an attacking posture, and male B attempted to retreat. But when he moved the two tubes into male B's territory, the tables were turned. By simply moving the two tubes from one end of the tank to the other, Tinbergen was able to dictate which male attacked and which retreated. Both males were evidently playing the simple conditional strategy: 'if resident, attack; if intruder, retreat.'

G E N E S M A N S H I P

I am an animal who has found a clump of eight mushrooms. After taking account of their nutritional value, and subtracting something for the slight risk that they might be poisonous, I estimate that they are worth +6 units each (the units are arbitrary pay-offs as in the previous chapter). The mushrooms are so big I could eat only three of them. Should I inform anybody else about my find, by giving a 'food call'? Who is within earshot? Brother B (his relatedness to me is 2), cousin C (relatedness to me = 1/8), and D (no particular relation: his relatedness to me is some small number which can be treated as zero for practical purposes). The net benefit score to me if I keep quiet about my find will be +6 for each of the three mushrooms I eat, that is +18 in all. My net benefit score if I give the food call needs a bit of figuring. The eight mushrooms will be shared equally between the four of us. The pay-off to me from the two that I eat myself will be the full +6 units each, that is +12 in all. But I shall also get some pay-off when my brother and cousin eat their two mushrooms each, because of our shared genes. The actual score comes to (1 x 12) + (1/2 x 12) + (1/8 x 12) + (0 x 12) = + 19.5. The corresponding net benefit for the selfish behaviour was +18: it is a closerun thing, but the verdict is clear. I should give the food call; altruism on my part would in this case pay my selfish genes.

In any case the calculation is only a very preliminary first approximation to what it ideally should be. It neglects many things, including the ages of the individuals concerned. Also, if I have just had a good meal, so that I can only find room for one mushroom, the net benefit of giving the food call will be greater than it would be if I was famished. There is no end to the progressive refinements of the calculation that could be achieved in the best of all possible worlds. But real life is not lived in the best of all possible worlds. We cannot expect real animals to take every last detail into account in coming to an optimum decision. We shall have to discover, by observation and experiment in the wild, how closely real animals actually come to achieving an ideal cost-benefit analysis.

In a species whose members do not move around much, or whose members move around in small groups, the chances may be good that any random individual you come across is fairly close kin to you. In this case the rule 'Be nice to any member of the species whom you meet' could have positive survival value, in the sense that a gene predisposing its possessors to obey the rule might become more numerous in the gene pool. This may be why altruistic behaviour is so frequently reported in troops of monkeys and schools of whales. Whales and dolphins drown if they are not allowed to breathe air. Baby whales, and injured individuals who cannot swim to the surface have been seen to be rescued and held up by companions in the school. It is not known whether whales have ways of knowing who their close relatives are, but it is possible that it does not matter. It may be that the overall probability that a random member of the school is a relation is so high that the altruism is worth the cost. Incidentally, there is at least one well-authenticated story of a drowning human swimmer being rescued by a wild dolphin. This could be regarded as a misfiring of the rule for saving drowning members of the school. The rule's 'definition' of a member of the school who is drowning might be something like: 'A long thing thrashing about and choking near the surface.'

Baby chicks feed in family clutches, all following their mother. They have two main calls. In addition to the loud piercing cheep which I have already mentioned, they give short melodious twitters when feeding. The cheeps, which have the effect of summoning the mother's aid, are ignored by the other chicks. The twitters, however, are attractive to chicks. This means that when one chick finds food, its twitters attract other chicks to the food as well: in the terms of the earlier hypothetical example, the twitters are 'food calls'. As in that case, the apparent altruism of the chicks can easily be explained by kin selection. Since, in nature, the chicks would be all full brothers and sisters, a gene for giving the food twitter would spread, provided the cost to the twitterer is less than half the net benefit to the other chicks. As the benefit is shared out between the whole clutch, which normally numbers more than two, it is not difficult to imagine this condition being realized.

An example of a deliberately engineered misfiring of the maternal instinct is provided by cuckoos, and other 'brood-parasites'-birds that lay their eggs in somebody else's nest. Cuckoos exploit the rule built into bird parents: 'Be nice to any small bird sitting in the nest that you built.' Cuckoos apart, this rule will normally have the desired effect of restricting altruism to immediate kin, because it happens to be a fact that nests are so isolated from each other that the contents of your own nest are almost bound to be your own chicks. Adult herring gulls do not recognize their own eggs, and will happily sit on other gull eggs, and even crude wooden dummies if these are substituted by a human experimenter. In nature, egg recognition is not important for gulls, because eggs do not roll far enough to reach the vicinity of a neighbour's nest, some yards away. Gulls do, however, recognize their own chicks: chicks, unlike eggs, wander, and can easily end up near the nest of a neighbouring adult, often with fatal results, as we saw in Chapter 1. Guillemots, on the other hand, do recognize their own eggs by means of the speckling pattern, and actively discriminate in favour of them when incubating. This is presumably because they nest on flat rocks, where there is a danger of eggs rolling around and getting muddled up. Now, it might be said, why do they bother to discriminate and sit only on their own eggs? Surely if everybody saw to it that she sat on somebody's egg, it would not matter whether each particular mother was sitting on her own or somebody else's. This is the argument of a group selectionist. Just consider what would happen if such a group baby-sitting circle did develop. The average clutch size of the guillemot is one. This means that if the mutual baby-sitting circle is to work successfully, every adult would have to sit on an average of one egg. Now suppose somebody cheated, and refused to sit on an egg. Instead of wasting time sitting, she could spend her time laying more eggs. And the beauty of the scheme is that the other, more altruistic, adults would look after them for her. They would go on faithfully obeying the rule 'If you see a stray egg near your nest, haul it in and sit on it.' So the gene for cheating the system would spread through the population, and the nice friendly baby-sitting circle would break down.

The song-bird species that are parasitized by cuckoos have fought back, not in this case by learning the appearance of their own eggs, but by discriminating instinctively in favour of eggs with the species-typical markings. Since they are not in danger of being parasitized by members of their own species, this is effective. But the cuckoos have retaliated in their turn by making their eggs more and more like those of the host species in colour, size, and markings. This is an example of a lie, and it often works. The result of this evolutionary arms race has been a remarkable perfection of mimicry on the part of the cuckoo eggs. We may suppose that a proportion of cuckoo eggs and chicks are 'found out', and those that are not found out are the ones who live to lay the next generation of cuckoo eggs. So genes for more effective deception spread through the cuckoo gene pool. Similarly, those host birds with eyes sharp enough to detect any slight imperfection in the cuckoo eggs' mimicry are the ones that contribute most to their own gene pool. Thus sharp and sceptical eyes are passed on to their next generation. This is a good example of how natural selection can sharpen up active discrimination, in this case discrimination against another species whose members are doing their best to foil the discriminators.

In many species a mother can be more sure of her young than a father can. The mother lays the visible, tangible egg, or bears the child. She has a good chance of knowing for certain the bearers of her own genes. The poor father is much more vulnerable to deception. It is therefore to be expected that fathers will put less effort than mothers into caring for young.

Returning to the fact that parental altruism is more common than fraternal altruism, it does seem reasonable to explain this in terms of the 'identification problem'. But this does not explain the fundamental asymmetry in the parent/child relationship itself. Parents care more for their children than children do for their parents, although the genetic relationship is symmetrical, and certainty of relatedness is just as great both ways. One reason is that parents are in a better practical position to help their young, being older and more competent at the business of living. Even if a baby wanted to feed its parents, it is not well equipped to do so in practice.

There is another asymmetry in the parent/child relationship which does not apply to the brother/sister one. Children are always younger than their parents. This often, though not always means they have a longer expectation of life. As I emphasized above, expectation of life is an important variable which, in the best of all possible worlds, should enter into an animal's 'calculation' when it is 'deciding' whether to behave altruistically or not. In a species in which children have a longer average life expectancy than parents, any gene for child altruism would be labouring under a disadvantage. It would be engineering altruistic self-sacrifice for the benefit of individuals who are nearer to dying of old age than the altruist itself. A gene for parent altruism, on the other hand, would have a corresponding advantage as far as the life-expectancy terms in the equation were concerned.

B A T T L E O F T H E G E N E R A T I O N S

This seems a good moment to mention the puzzling phenomenon known as the menopause, the rather abrupt termination of a human female's reproductive fertility in middle age. This may not have occurred too commonly in our wild ancestors, since not many women would have lived that long anyway. But still, the difference between the abrupt change of life in women and the gradual fading out of fertility in men suggests that there is something genetically 'deliberate' about the menopause-that it is an 'adaptation'. It is rather difficult to explain. At first sight we might expect that a woman should go on having children until she dropped, even if advancing years made it progressively less likely that any individual child would survive. Surely it would seem always worth trying? But we must remember that she is also related to her grandchildren, though half as closely.

For various reasons, perhaps connected with the Medawar theory of ageing, women in the natural state became gradually less efficient at bringing up children as they got older. Therefore the life expectancy of a child of an old mother was less than that of a child of a young mother. This means that, if a woman had a child and a grandchild born on the same day, the grandchild could expect to live longer than the child. When a woman reached the age where the average chance of each child reaching adulthood was just less than half the chance of each grandchild of the same age reaching adulthood, any gene for investing in grandchildren in preference to children would tend to prosper. Such a gene is carried by only one in four grandchildren, whereas the rival gene is carried by one in two children, but the greater expectation of life of the grandchildren outweighs this, and the 'grandchild altruism' gene prevails in the gene pool. A woman could not invest fully in her grandchildren if she went on having children of her own. Therefore genes for becoming reproductively infertile in middle age became more numerous, since they were carried in the bodies of grandchildren whose survival was assisted by grandmotherly altruism. This is a possible explanation of the evolution of the menopause in females. The reason why the fertility of males tails off gradually rather than abruptly is probably that males do not invest so much as females in each individual child anyway. Provided he can sire children by young women, it will always pay even a very old man to invest in children rather than in grandchildren.

A. Zahavi has suggested a particularly diabolical form of child blackmail: the child screams in such a way as to attract predators deliberately to the nest. The child is 'saying' 'Fox, fox, come and get me.' The only way the parent can stop it screaming is to feed it. So the child gains more than its fair share of food, but at a cost of some risk to itself. The principle of this ruthless tactic is the same as that of the hijacker threatening to blow up an aeroplane, with himself on board, unless he is given a ransom.

Cuckoo genes for screaming loudly became more numerous in the cuckoo gene pool because the loud screams increased the probability that the foster parents would feed the baby cuckoos. The reason the foster parents responded to the screams in this way was that genes for responding to the screams had spread through the gene pool of the foster-species. The reason these genes spread was that individual foster parents who did not feed the cuckoos extra food, reared fewer of their own children-fewer than rival parents who did feed their cuckoos extra. This was because predators were attracted to the nest by the cuckoo cries. Although cuckoo genes for not screaming were less likely to end up in the bellies of predators than screaming genes, the non-screaming cuckoos paid the greater penalty of not being fed extra rations. Therefore the screaming genes spread through the cuckoo gene pool.

There is no evidence, one way or the other, on whether cuckoos, and other birds of similar 'brood-parasitic' habit, actually employ the blackmail tactic. But they certainly do not lack ruthlessness. For instance, there are honey-guides who, like cuckoos, lay their eggs in the nests of other species. The baby honey-guide is equipped with a sharp, hooked beak. As soon as he hatches out, while he is still blind, naked, and otherwise helpless, he scythes and slashes his foster brothers and sisters to death: dead brothers do not compete for food! The familiar British cuckoo achieves the same result in a slightly different way. It has a short incubation-time, and so the baby cuckoo manages to hatch out before its foster brothers and sisters. As soon as it hatches, blindly and mechanically, but with devastating effectiveness, it throws the other eggs out of the nest. It gets underneath an egg, fitting it into a hollow in its back. Then it slowly backs up the side of the nest, balancing the egg between its wing-stubs, and topples the egg out on to the ground. It does the same with all the other eggs, until it has the nest, and therefore the attention of its foster parents, entirely to itself.

B A T T L E O F T H E S E X E S

In certain primitive organisms, for instance some fungi, maleness and femaleness do not occur, although sexual reproduction of a kind does. In the system known as isogamy the individuals are not distinguishable into two sexes. Anybody can mate with anybody else. There are not two different sorts of gametes-sperms and eggs-but all sex cells are the same, called isogametes. New individuals are formed by the fusion of two isogametes, each produced by meiotic division. If we have three isogametes, A, B, and C,

A could fuse with B or C,

B could fuse with A or C.

The same is never true of normal sexual systems. If A is a sperm and it can fuse with B or C, then B and C must be eggs and B cannot fuse with C.

When two isogametes fuse, both contribute equal numbers of genes to the new individual, and they also contribute equal amounts of food reserves. Sperms and eggs too contribute equal numbers of genes, but eggs contribute far more in the way of food reserves: indeed, sperms make no contribution at all and are simply concerned with transporting their genes as fast as possible to an egg. At the moment of conception, therefore, the father has invested less than his

fair share (i.e. 50 per cent) of resources in the offspring. Since each sperm is so tiny, a male can afford to make many millions of them every day. This means he is potentially able to beget a very large number of children in a very short period of time, using different females. This is only possible because each new embryo is endowed with adequate food by the mother in each case. This therefore places a limit on the number of children a female can have, but the number of children a male can have is virtually unlimited. Female exploitation begins here.

Parker and others showed how this asymmetry might have evolved from an originally isogamous state of affairs. In the days when all sex cells were interchangeable and of roughly the same size, there would have been some that just happened to be slightly bigger than others. In some respects a big isogamete would have an advantage over an average-sized one, because it would get its embryo off to a good start by giving it a large initial food supply. There might therefore have been an evolutionary trend towards larger gametes. But there was a catch. The evolution of isogametes that were larger than was strictly necessary would have opened the door to selfish exploitation. Individuals who produced smaller than average gametes could cash in, provided they could ensure that their small gametes fused with extra-big ones. This could be achieved by making the small ones more mobile, and able to seek out large ones actively. The advantage to an individual of producing small, rapidly moving gametes would be that he could afford to make a larger number of gametes, and therefore could potentially have more children. Natural selection favoured the production of sex cells that were small and that actively sought out big ones to fuse with. So we can think of two divergent sexual 'strategies' evolving. There was the large-investment or 'honest' strategy. This automatically opened the way for a smallinvestment exploitative strategy. Once the divergence between the two strategies had started, it would have continued in runaway fashion.

Medium-sized intermediates would have been penalized, because they did not enjoy the advantages of either of the two more extreme strategies. The exploiters would have evolved smaller and smaller size, and faster mobility. The honest ones would have evolved larger and larger size, to compensate for the ever-smaller investment contributed by the exploiters, and they became immobile because they would always be actively chased by the exploiters anyway. Each honest one would 'prefer' to fuse with another honest one. But the selection pressure to lock out exploiters would have been weaker than the pressure on exploiters to duck under the barrier: the exploiters had more to lose, and they therefore won the evolutionary battle. The honest ones became eggs, and the exploiters became sperms.

In mammals, sex is determined genetically as follows. All eggs are capable of developing into either a male or a female. It is the sperms that carry the sex-determining chromosomes. Half the sperms produced by a man are female-producing, or X-sperms, and half are male-producing, or Y-sperms. The two sorts of sperms look alike. They differ with respect to one chromosome only. A gene for making a father have nothing but daughters could achieve its object by making him manufacture nothing but X-sperms. A gene for making a mother have nothing but daughters could work by making her secrete a selective spermicide, or by making her abort male embryos.

Consider again the mated pair with which we began the chapter. Both partners, as selfish machines, 'want' sons and daughters in equal numbers. To this extent they agree. Where they disagree is in who is going to bear the brunt of the cost of rearing each one of those children. Each individual wants as many surviving children as possible. The less he or she is obliged to invest in any one of those children, the more children he or she can have. The obvious way to achieve this desirable state of affairs is to induce your sexual partner to invest more than his or her fair share of resources in each child, leaving you free to have other children with other partners. This would be a desirable strategy for either sex, but it is more difficult for the female to achieve. Since she starts by investing more than the male, in the form of her large, food-rich egg, a mother is already at the moment of conception 'committed' to each child more deeply than the father is. She stands to lose more if the child dies than the father does. More to the point, she would have to invest more than the father in the future in order to bring a new substitute child up to the same level of development. If she tried the tactic of leaving the father holding the baby, while she went off with another male, the father might, at relatively small cost to himself, retaliate by abandoning the baby too. Therefore, at least in the early stages of child development, if any abandoning is going to be done, it is likely to be the father who abandons the mother rather than the other way around. Similarly, females can be expected to invest more in children than males, not only at the outset, but throughout development. So, in mammals for example, it is the female who incubates the foetus in her own body, the female who makes the milk to suckle it when it is born, the female who bears the brunt of the load of bringing it up and protecting it. The female sex is exploited, and the fundamental evolutionary basis for the exploitation is the fact that eggs are larger than sperms.

Of course in many species the father does work hard and faithfully at looking after the young. But even so, we must expect that there will normally be some evolutionary pressure on males to invest a little bit less in each child, and to try to have more children by different wives. By this I simply mean that there will be a tendency for genes that say 'Body, if you are male leave your mate a little bit earlier than my rival allele would have you do, and look for another female', to be successful in the gene pool. The extent to which this evolutionary pressure actually prevails in practice varies greatly from species to species. In many, for example in the birds of paradise, the female receives no help at all from any male, and she rears her children on her own. Other species such as kittiwakes form monogamous pairbonds of exemplary fidelity, and both partners cooperate in the work of bringing up children. Here we must suppose that some evolutionary counter-pressure has been at work: there must be a penalty attached to the selfish mate-exploitation strategy as well as a benefit, and in kittiwakes the penalty outweighs the benefit. It will in any case only pay a father to desert his wife and child if the wife has a reasonable chance of rearing the child on her own. Trivers has considered the possible courses of action open to a mother who has been deserted by her mate. Best of all for her would be to try to deceive another male into adopting her child, 'thinking' it is his own. This might not be too difficult if it is still a foetus, not yet born. Of course, while the child bears half her genes, it bears no genes at all from the gullible step-father. Natural selection would severely penalize such gullibility in males and indeed would favour males who took active steps to kill any potential step-children as soon as they mated with a new wife. This is very probably the explanation of the so-called Bruce effect: male mice secrete a chemical which when smelt by a pregnant female can cause her to abort. She only aborts if the smell is different from that of her former mate. In this way. a male mouse destroys his potential stepchildren, and renders his new wife receptive to his own sexual advances. Ardrey, incidentally, sees the Bruce effect as a population control mechanism! A similar example is that of male lions, who, when newly arrived in a pride, sometimes murder existing cubs, presumably because these are not their own children.

A male can achieve the same result without necessarily killing stepchildren. He can enforce a period of prolonged courtship before he copulates with a female, driving away all other males who approach her,and preventing her from escaping. In this way he can wait and see whether she is harbouring any little step-children in her womb, and desert her if so. We shall see below a reason why a female might want a long 'engagement' period before copulation. Here we have a reason why a male might want one too. Provided he can isolate her from all contact with other males, it helps to avoid being the unwitting benefactor of another male's children. Assuming then that a deserted female cannot fool a new male into adopting her child, what else can she do? Much may depend on how old the child is. If it is only just conceived, it is true that she has invested the whole of one egg in it and perhaps more, but it may still pay her to abort it and find a new mate as quickly as possible. In these circumstances it would be to the mutual advantage both of her and of the potential new husband that she should abort-since we are assuming she has no hope of fooling him into adopting the child. This could explain why the Bruce effect works from the female's point of view. Another option open to a deserted female is to stick it out, and try and rear the child on her own. This will especially pay her if the child is already quite old. The older he is the more has already been invested in him, and the less it will take out of her to finish the job of rearing him. Even if he is still quite young, it might yet pay her to try to salvage something from her initial investment, even if she has to work twice as hard to feed the child, now that the male has gone. It is no comfort to her that the child contains half the male's genes too, and that she could spite him by abandoning it. There is no point in spite for its own sake. The child carries half her genes, and the dilemma is now hers alone. Paradoxically, a reasonable policy for a female who is in danger of being deserted might be to walk out on the male before he walks out on her. This could pay her, even if she has already invested more in the child than the male has. The unpleasant truth is that in some circumstances an advantage accrues to the partner who deserts first, whether it is the father or the mother. As Trivers puts it, the partner who is left behind is placed in a cruel bind. It is a rather horrible but very subtle argument. A parent may be expected to desert, the moment it is possible for him or her to say the following: ' This child is now far enough developed that either of us could finish off rearing it on our own. Therefore it would pay me to desert now, provided I could be sure my partner would not desert as well. If I did desert now, my partner would do whatever is best for her/his genes. He/ she would be forced into making a more drastic decision than I am making now, because I would have already left. My partner would "know" that if he/she left as well, the child would surely die. Therefore, assuming that my partner will take the decision that is best for his/her own selfish genes, I conclude that my own best course of action is to desert first. This is especially so, since my partner may be "thinking" along exactly the same lines, and may seize the initiative at any minute by deserting me!' As always, the subjective soliloquy is intended for illustration only. The point is that genes for deserting first could be favourably selected simply because genes for deserting second would not be.

We have looked at some of the things that a female might do if she has been deserted by her mate. But these all have the air of making the best of a bad job. Is there anything a female can do to reduce the extent to which her mate exploits her in the first place? She has a strong card in her hand. She can refuse to copulate. She is in demand, in a seller's market. This is because she brings the dowry of a large, nutritious egg. A male who successfully copulates gains a valuable food reserve for his offspring. The female is potentially in a position to drive a hard bargain before she copulates. Once she has copulated she has played her ace-her egg has been committed to the male. It is all very well to talk about driving hard bargains, but we know very well it is not really like that. Is there any realistic way in which something equivalent to driving a hard bargain could evolve by natural selection? I shall consider two main possibilities, called the domestic-bliss strategy, and the he-man strategy. The simplest version of the domestic-bliss strategy is this. The female looks the males over, and tries to spot signs of fidelity and domesticity in advance. There is bound to be variation in the population of males in their predisposition to be faithful husbands. If females could recognize such qualities in advance, they could benefit themselves by choosing males possessing them. One way for a female to do this is to play hard to get for a long time, to be coy. Any male who is not patient enough to wait until the female eventually consents to copulate is not likely to be a good bet as a faithful husband. By insisting on a long engagement period, a female weeds out casual suitors, and only finally copulates with a male who has proved his qualities of fidelity and perseverance in advance. Feminine coyness is in fact very common among animals, and so are prolonged courtship or engagement periods. As we have already seen, a long engagement can also benefit a male where there is a danger of his being duped into caring for another male's child. Courtship rituals often include considerable pre-copulation investment by the male. The female may refuse to copulate until the male has built her a nest. Or the male may have to feed her quite substantial amounts of food. This, of course, is very good from the female's point of view, but it also suggests another possible version of the domestic-bliss strategy. Could females force males to invest so heavily in their offspring before they allow copulation that it would no longer pay the males to desert after copulation? The idea is appealing. A male who waits for a coy female eventually to copulate with him is paying a cost: he is forgoing the chance to copulate with other females, and he is spending a lot of time and energy in courting her. By the time he is finally allowed to copulate with a particular female, he will inevitably be heavily 'committed' to her. There will be little temptation for him to desert her, if he knows that any future female he approaches will also procrastinate in the same manner before she will get down to business.

As I showed in a paper, there is a mistake in Trivers's reasoning here. He thought that prior investment in itself committed an individual to future investment. This is fallacious economics. A business man should never say 'I have already invested so much in the Concorde airliner (for instance) that I cannot afford to scrap it now.' He should always ask instead whether it would pay him in the future, to cut his losses, and abandon the project now, even though he has already invested heavily in it. Similarly, it is no use a female forcing a male to invest heavily in her in the hope that this, on its own, will deter the male from subsequently deserting. This version of the domestic-bliss strategy depends upon one further crucial assumption. This is that a majority of the females can be relied upon to play the same game. If there are loose females in the population, prepared to welcome males who have deserted their wives, then it could pay a male to desert his wife, no matter how much he has already invested in her children.

Much therefore depends on how the majority of females behave. If we were allowed to think in terms of a conspiracy of females there would be no problem. But a conspiracy of females can no more evolve than the conspiracy of doves which we considered under "AGGRESSION:". Instead, we must look for evolutionarily stable strategies. Let us take Maynard Smith's method of analysing aggressive contests, and apply it to sex. It will be a little bit more complicated than the case of the hawks and doves, because we shall have two female strategies and two male strategies. As in Maynard Smith's studies, the word 'strategy' refers to a blind unconscious behaviour program. Our two female strategies will be called coy and fast, and the two male strategies will be called faithful and philanderer. The behavioural rules of the four types are as follows. Coy females will not copulate with a male until he has gone through a long and expensive courtship period lasting several weeks. Fast females will copulate immediately with anybody. Faithful males are prepared to go on courting for a long time, and after copulation they stay with the female and help her to rear the young. Philanderer males lose patience quickly if a female will not copulate with them straight away: they go off and look for another female; after copulation too they do not stay and act as good fathers, but go off in search of fresh females. As in the case of the hawks and doves, these are not the only possible strategies, but it is illuminating to study their fates nevertheless.

Like Maynard Smith, we shall use some arbitrary hypothetical values for the various costs and benefits. To be more general it can be done with algebraic symbols, but numbers are easier to understand. Suppose that the genetic pay-off gained by each parent when a child is reared successfully is +15 units. The cost of rearing one child, the cost of all its food, all the time spent looking after it, and all the risks taken on its behalf, is -20 units. The cost is expressed as negative, because it is 'paid out' by the parents. Also negative is the cost of wasting time in prolonged courtship. Let this cost be -3 units.

Imagine we have a population in which all the females are coy, and all the males are faithful. It is an ideal monogamous society. In each couple, the male and the female both get the same average pay-off. They get +15 for each child reared; they share the cost of rearing it (-20) equally between the two of them, an average of -10 each. They both pay the -3 point penalty for wasting time in prolonged courtship. The average payoff for each is therefore + 15 - 10 - 3 = + 2.

Now suppose a single fast female enters the population. She does very well. She does not pay the cost of delay, because she does not indulge in prolonged courtship. Since all the males in the population are faithful, she can reckon on finding a good father for her children whoever she mates with. Her average pay-off per child is + 15 - 10 = + 5. She is 3 units better off than her coy rivals. Therefore fast genes will start to spread. If the success of fast females is so great that they come to predominate in the population, things will start to change in the male camp too. So far, faithful males have had a monopoly. But now if a philanderer male arises in the population, he starts to do better than his faithful rivals. In a population where all the females are fast, the pickings for a philanderer male are rich indeed. He gets the +15 points if a child is successfully reared, and he pays neither of the two costs. What this lack of cost mainly means to him is that he is free to go off and mate with new females. Each of his unfortunate wives struggles on alone with the child, paying the entire -20 point cost, although she does not pay anything for wasting time in courting. The net pay-off for a fast female when she encounters a philanderer male is + 15 - 20 = -5; the pay-off to the philanderer himself is +15. In a population in which all the females are fast, philanderer genes will spread like wildfire. If the philanderers increase so successfully that they come to dominate the male part of the population, the fast females will be in dire straits. Any coy female would have a strong advantage. If a coy female encounters a philanderer male, no business results. She insists on prolonged courtship; he refuses and goes off in search of another female. Neither partner pays the cost of wasting time. Neither gains anything either, since no child is produced. This gives a net pay-off of zero for a coy female in a population where all the males are philanderers. Zero may not seem much, but it is better than the -5 which is the average score for a fast female. Even if a fast female decided to leave her young after being deserted by a philanderer, she would still have paid the considerable cost of an egg. So, coy genes start to spread through the population again.

To complete the hypothetical cycle, when coy females increase in numbers so much that they predominate, the philanderer males, who had such an easy time with the fast females, start to feel the pinch. Female after female insists on a long and arduous courtship. The philanderers flit from female to female, and always the story is the same. The net pay-off for a philanderer male when all the females are coy is zero. Now if a single faithful male should turn up, he is the only one with whom the coy females will mate. His net pay-off is + 2, better than that of the philanderers. So, faithful genes start to increase, and we come full circle.

A female, playing the domestic-bliss strategy, who simply looks the males over and tries to recognize qualities of fidelity in advance, lays herself open to deception. Any male who can pass himself off as a good loyal domestic type, but who in reality is concealing a strong tendency towards desertion and unfaithfulness, could have a great advantage. As long as his deserted former wives have any chance of bringing up some of the children, the philanderer stands to pass on more genes than a rival male who is an honest husband and father. Genes for effective deception by males will tend to be favoured in the gene pool. Conversely, natural selection will tend to favour females who become good at seeing through such deception. One way they can do this is to play especially hard to get when they are courted by a new male, but in successive breeding seasons to be increasingly ready to accept quickly the advances of last year's mate. This will automatically penalize young males embarking on their first breeding season, whether they are deceivers or not. The brood of naive first year females would tend to contain a relatively high proportion of genes from unfaithful fathers, but faithful fathers have the advantage in the second and subsequent years of a mother's life, for they do not have to go through the same prolonged energy-wasting and time-consuming courtship rituals. If the majority of individuals in a population are the children of experienced rather than naive mothers-a reasonable assumption in any long-lived species- genes for honest, good fatherhood will come to prevail in the gene pool.

There are species, however, in which the male actually does more work in caring for the children than the female does. Among birds and mammals these cases of paternal devotion are exceptionally rare, but they are common among fish. Why? This is a challenge for the selfish gene theory which has puzzled me for a long time. An ingenious solution was recently suggested to me in a tutorial by Miss T. R. Carlisle. She makes use of Trivers's 'cruel bind' idea, referred to above, as follows. Many fish do not copulate, but instead simply spew out their sex cells into the water. Fertilization takes place in the open water, not inside the body of one of the partners. This is probably how sexual reproduction first began. Land animals like birds, mammals and reptiles, on the other hand, cannot afford this kind of external fertilization, because their sex cells are too vulnerable to drying-up. The gametes of one sex-the male, since sperms are mobile-are introduced into the wet interior of a member of the other sex-the female. So much is just fact. Now comes the idea. After copulation, the land-dwelling female is left in physical possession of the embryo. It is inside her body. Even if she lays the fertilized egg almost immediately, the male still has time to vanish, thereby forcing the female into Trivers's 'cruel bind'. The male is inevitably provided with an opportunity to take the prior decision to desert, closing the female's options, and forcing her to decide whether to leave the young to certain death, or whether to stay with it and rear it. Therefore, maternal care is more common among land animals than paternal care. But for fish and other water-dwelling animals things are very different. If the male does not physically introduce his sperms into the female's body there is no necessary sense in which the female is left 'holding the baby'.

Either partner might make a quick getaway and leave the other one in possession of the newly fertilized eggs. But there is even a possible reason why it might often be the male who is most vulnerable to being deserted. It seems probable that an evolutionary battle will develop over who sheds their sex cells first. The partner who does so has the advantage that he or she can then leave the other one in possession of the new embryos. On the other hand, the partner who spawns first runs the risk that his prospective partner may subsequently fail to follow suit. Now the male is more vulnerable here, if only because sperms are lighter and more likely to diffuse than eggs. If a female spawns too early, i.e. before the male is ready, it will not greatly matter because the eggs, being relatively large and heavy, are likely to stay together as a coherent clutch for some time. Therefore a female fish can afford to take the 'risk' of spawning early. The male dare not take this risk, since if he spawns too early his sperms will have diffused away before the female is ready, and she will then not spawn herself, because it will not be worth her while to do so. Because of the diffusion problem, the male must wait until the female spawns, and then he must shed his sperms over the eggs. But she has had a precious few seconds in which to disappear, leaving the male in possession, and forcing him on to the horns of Trivers's dilemma. So this theory neatly explains why paternal care is common in water but rare on dry land.

Because a male produces many millions of sperms to every egg produced by a female, sperms heavily outnumber eggs in the population. Any given egg is therefore much more likely to enter into sexual fusion than any given sperm is. Eggs are a relatively valuable resource, and therefore a female does not need to be so sexually attractive as a male does in order to ensure that her eggs are fertilized.

Y O U S C R A T C H M Y B A C K, I ' L L R I D E O N Y O U R S

What is it about the idea of a god that gives it its stability and penetrance in the cultural environment? The survival value of the god meme in the meme pool results from its great psychological appeal. It provides a superficially plausible answer to deep and troubling questions about existence. It suggests that injustices in this world may be rectified in the next. The 'everlasting arms' hold out a cushion against our own inadequacies which, like a doctor's placebo, is none the less effective for being imaginary.

N I C E G U Y S F I N I S H F I R S T

Nobody would ever claim that a bacterium was a conscious strategist, yet bacterial parasites are probably engaged in ceaseless games of Prisoner's Dilemma with their hosts and there is no reason why we should not attribute Axelrodian adjectives-forgiving, non-envious, and so on-to their strategies. Axelrod and Hamilton point out that normally harmless or beneficial bacteria can turn nasty, even causing lethal sepsis, in a person who is injured. A doctor might say that the person's 'natural resistance' is lowered by the injury. But perhaps the real reason is to do with games of Prisoner's Dilemma. Do the bacteria, perhaps, have something to gain, but usually keep themselves in check? In the game between human and bacteria, the 'shadow of the future' is normally long since a typical human can be expected to live for years from any given starting-point. A seriously wounded human, on the other hand, may present a potentially much shorter shadow of the future to his bacterial guests. The 'Temptation to defect' correspondingly starts to look like a more attractive option than the 'Reward for mutual cooperation'. Needless to say, there is no suggestion that the bacteria work all this out in their nasty little heads! Selection on generations of bacteria has presumably built into them an unconscious rule of thumb which works by purely biochemical means.

Plants, according to Axelrod and Hamilton, may even take revenge, again obviously unconsciously. Fig trees and fig wasps share an intimate cooperative relationship. The fig that you eat is not really a fruit. There is a tiny hole at the end, and if you go into this hole (you'd have to be as small as a fig wasp to do so, and they are minute: thankfully too small to notice when you eat a fig), you find hundreds of tiny flowers lining the walls. The fig is a dark indoor hothouse for flowers, an indoor pollination chamber. And the only agents that can do the pollinating are fig wasps. The tree, then, benefits from harbouring the wasps. But what is in it for the wasps? They lay their eggs in some of the tiny flowers, which the larvae then eat. They pollinate other flowers within the same fig. 'Defecting', for a wasp, would mean laying eggs in too many of the flowers in a fig and pollinating too few of them. But how could a fig tree 'retaliate'? According to Axelrod and Hamilton, 'It turns out in many cases that if a fig wasp entering a young fig does not pollinate enough flowers for seeds and instead lays eggs in almost all, the tree cuts off the developing fig at an early stage. All progeny of the wasp then perish.'

A bizarre example of what appears to be a Tit for Tat arrangement in nature was discovered by Eric Fischer in a hermaphrodite fish, the sea bass. Unlike us, these fish don't have their sex determined at conception by their chromosomes. Instead, every individual is capable of performing both female and male functions. In any one spawning episode they shed either eggs or sperm. They form monogamous pairs and, within the pair, take turns to play the male and female roles. Now, we may surmise that any individual fish, if it could get away with it, would 'prefer' to play the male role all the time, because the male role is cheaper. Putting it another way, an individual that succeeded in persuading its partner to play the female most of the time would gain all the benefits of 'her' economic investment in eggs, while 'he' has resources left over to spend on other things, for instance on mating with other fish.

In fact, what Fischer observed was that the fishes operate a system of pretty strict alternation. This is just what we should expect if they are playing Tit for Tat. And it is plausible that they should, because it does appear that the game is a true Prisoner's Dilemma, albeit a somewhat complicated one. To play the cooperate card means to play the female role when it is your turn to do so. Attempting to play the male role when it is your turn to play the female is equivalent to playing the defect card. Defection is vulnerable to retaliation: the partner can refuse to play the female role next time it is 'her' (his?) turn to do so, or 'she' can simply terminate the whole relationship. Fischer did indeed observe that pairs with an uneven sharing of sex roles tended to break up.

T H E L O N G R E A C H O F T H E G E N E

On 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. Darwinians have usually chosen to discuss genes whose phenotypic effects benefit, or penalize, the survival and reproduction of whole bodies. They 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. But 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. Cases 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. It 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. Throughout this book we have been alert to the possibility of individual organisms 'cheating' in subtle ways against their social companions. Here we are talking about single genes cheating against the other genes with which they share a body. The 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. How 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. Not all segregation distorters have such destructive side-effects as t.

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

The 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?

It 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.

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 nothappy 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.

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.

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 "YOU SCRATCH MY BACK..."). 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.