commonplace book redux

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? […]

I am using the word gene to mean a genetic unit that is small enough to last for a large number of generations and to be distributed around in the form of many copies. This is not a rigid all-or-nothing definition, but a kind of fading-out definition, like the definition of ‘big’ or ‘old’. The more likely a length of chromosome is to be split by crossing-over, or altered by mutations of various kinds, the less it qualifies to be called a gene in the sense in which I am using the term.

Following Williams, I made much of the fragmenting effects of meiosis in my argument that the individual organism cannot play the role of replicator in natural selection. I now see that this was only half the story. The other half is spelled out in The Extended Phenotype (pp. 97–9) and in my paper ‘Replicators and Vehicles’. If the fragmenting effects of meiosis were the whole story, an asexually reproducing organism like a female stick-insect would be a true replicator, a sort of giant gene. But if a stick insect is changed—say it loses a leg—the change is not passed on to future generations. Genes alone pass down the generations, whether reproduction is sexual or asexual. Genes, therefore, really are replicators. In the case of an asexual stick-insect, the entire genome (the set of all its genes) is a replicator. But the stick-insect itself is not. A stick-insect body is not moulded as a replica of the body of the previous generation. The body in any one generation grows afresh from an egg, under the direction of its genome, which is a replica of the genome of the previous generation. All printed copies of this book will be the same as one another. They will be replicas but not replicators. They will be replicas not because they have copied one another, but because all have copied the same printing plates. They do not form a lineage of copies, with some books being ancestral to others. A lineage of copies would exist if we xeroxed a page of a book, then xeroxed the xerox, then xeroxed the xerox of the xerox, and so on. In this lineage of pages, there really would be an ancestor/descendant relationship. A new blemish that showed up anywhere along the series would be shared by descendants but not by ancestors. An ancestor/descendant series of this kind has the potential to evolve. Superficially, successive generations of stick-insect bodies appear to constitute a lineage of replicas. But if you experimentally change one member of the lineage (for instance by removing a leg), the change is not passed on down the lineage. By contrast, if you experimentally change one member of the lineage of genomes (for instance by X-rays), the change will be passed on down the lineage. This, rather than the fragmenting effect of meiosis, is the fundamental reason for saying that the individual organism is not the ‘unit of selection’—not a true replicator. It is one of the most important consequences of the universally admitted fact that the ‘Lamarckian’ theory of inheritance is false.

Just as it is not convenient to talk about quanta and fundamental particles when we discuss the workings of a car, so it is often tedious and unnecessary to keep dragging genes in when we discuss the behaviour of survival machines. In practice it is usually convenient, as an approximation, to regard the individual body as an agent ‘trying’ to increase the numbers of all its genes in future generations. […]

It is theoretically possible that a gene could arise which conferred an externally visible ‘label’, say a pale skin, or a green beard, or anything conspicuous, and also a tendency to be specially nice to bearers of that conspicuous label. It is possible, but not particularly likely. Green beardedness is just as likely to be linked to a tendency to develop ingrowing toenails or any other trait, and a fondness for green beards is just as likely to go together with an inability to smell freesias. It is not very probable that one and the same gene would produce both the right label and the right sort of altruism. Nevertheless, what may be called the Green Beard Altruism Effect is a theoretical possibility. […]

There is an even more serious shortcoming in Wilson’s definition of kin selection. He deliberately excludes offspring: they don’t count as kin!* Now of course he knows perfectly well that offspring are kin to their parents, but he prefers not to invoke the theory of kin selection in order to explain altruistic care by parents of their own offspring. He is, of course, entitled to define a word however he likes, but this is a most confusing definition, and I hope that Wilson will change it in future editions of his justly influential book. Genetically speaking, parental care and brother/sister altruism evolve for exactly the same reason: in both cases there is a good chance that the altruistic gene is present in the body of the beneficiary. […]

There is one example of a mistake which is so extreme that you may prefer to regard it not as a mistake at all, but as evidence against the selfish gene theory. This is the case of bereaved monkey mothers who have been seen to steal a baby from another female, and look after it. I see this as a double mistake, since the adopter not only wastes her own time; she also releases a rival female from the burden of child-rearing, and frees her to have another child more quickly. It seems to me a critical example which deserves some thorough research. We need to know how often it happens; what the average relatedness between adopter and child is likely to be; and what the attitude of the real mother of the child is—it is, after all, to her advantage that her child should be adopted; do mothers deliberately try to deceive naive young females into adopting their children? (It has also been suggested that adopters and baby-snatchers might benefit by gaining valuable practice in the art of childrearing.) […]

So we conclude that the ‘true’ relatedness may be less important in the evolution of altruism than the best estimate of relatedness that animals can get. This fact is probably a key to understanding why parental care is so much more common and more devoted than brother/sister altruism in nature, and also why animals may value themselves more highly even than several brothers. Briefly, what I am saying is that, in addition to the index of relatedness, we should consider something like an index of ‘certainty’. Although the parent/child relationship is no closer genetically than the brother/sister relationship, its certainty is greater. It is normally possible to be much more certain who your children are than who your brothers are. And you can be more certain still who you yourself are! […]

I recommend Alan Grafen’s essay ‘Natural Selection, Kin Selection and Group Selection’ as a clear-thinking, and I hope now definitive, sorting out of the neo-group-selection problem. […]

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. […]

What Alexander is basically saying is this. A gene that made a child grab more than his fair share when he was a child, at the expense of his parent’s total reproductive output, might indeed increase his chances of surviving. But he would pay the penalty when he came to be a parent himself, because his own children would tend to inherit the same selfish gene, and this would reduce his overall reproductive success. He would be hoist with his own petard. Therefore the gene cannot succeed, and parents must always win the conflict. Our suspicions should be immediately aroused by this argument, because it rests on the assumption of a genetic asymmetry which is not really there. Alexander is using the words ‘parent’ and ‘offspring’ as though there was a fundamental genetic difference between them. As we have seen, although there are practical differences between parent and child, for instance parents are older than children, and children come out of parents’ bodies, there is really no fundamental genetic asymmetry. The relatedness is 50 per cent, whichever way round you look at it. To illustrate what I mean, I am going to repeat Alexander’s words, but with ‘parent’, ‘juvenile’ and other appropriate words reversed. ‘Suppose that a parent has a gene that tends to cause an even distribution of parental benefits. A gene which in this fashion improves an individual’s fitness when it is a parent could not fail to have lowered its fitness more when it was a juvenile.’ We therefore reach the opposite conclusion to Alexander, namely that in any parent/offspring conflict, the child must win! Obviously something is wrong here. Both arguments have been put too simply. The purpose of my reverse quotation is not to prove the opposite point to Alexander, but simply to show that you cannot argue in that kind of artificially asymmetrical way. Both Alexander’s argument, and my reversal of it, erred through looking at things from the point of view of an individual—in Alexander’s case, the parent, in my case, the child. I believe this kind of error is all too easy to make when we use the technical term ‘fitness’. This is why I have avoided using the word in this book. There is really only one entity whose point of view matters in evolution, and that entity is the selfish gene. Genes in juvenile bodies will be selected for their ability to outsmart parental bodies; genes in parental bodies will be selected for their ability to outsmart the young. There is no paradox in the fact that the very same genes successively occupy a juvenile body and a parental body. Genes are selected for their ability to make the best use of the levers of power at their disposal: they will exploit their practical opportunities. When a gene is sitting in a juvenile body its practical opportunities will be different from when it is sitting in a parental body. Therefore its optimum policy will be different in the two stages in its body’s life history. There is no reason to suppose, as Alexander does, that the later optimum policy should necessarily overrule the earlier. There is another way of putting the argument against Alexander. He is tacitly assuming a false asymmetry between the parent/child relationship on the one hand, and the brother/sister relationship on the other. You will remember that, according to Trivers, the cost to a selfish child of grabbing more than his share, the reason why he only grabs up to a point, is the danger of loss of his brothers and sisters who each bear half his genes. But brothers and sisters are only a special case of relatives with a 50 per cent relatedness. The selfish child’s own future children are no more and no less ‘valuable’ to him than his brothers and sisters. Therefore the total net cost of grabbing more than your fair share of resources should really be measured, not only in lost brothers and sisters, but also in lost future offspring due to their selfishness among themselves. Alexander’s point about the disadvantage of juvenile selfishness spreading to your own children, thereby reducing your own long-term reproductive output, is well taken, but it simply means we must add this in to the cost side of the equation. An individual child will still do well to be selfish so long as the net benefit to him is at least half the net cost to close relatives. But ‘close relatives’ should be read as including, not just brothers and sisters, but future children of one’s own as well. An individual should reckon his own welfare as twice as valuable as that of his brothers, which is the basic assumption Trivers makes. But he should also value himself twice as highly as one of his own future children. Alexander’s conclusion that there is a built-in advantage on the parent’s side in the conflict of interests is not correct.[…]

There is, then, no general answer to the question of who is more likely to win the battle of the generations. What will finally emerge is a compromise between the ideal situation desired by the child and that desired by the parent. It is a battle comparable to that between cuckoo and foster parent, not such a fierce battle to be sure, for the enemies do have some genetic interests in common—they are only enemies up to a point, or during certain sensitive times. However, many of the tactics used by cuckoos, tactics of deception and exploitation, may be employed by a parent’s own young, although the parent’s own young will stop short of the total selfishness that is to be expected of a cuckoo. […]

A male can achieve the same result without necessarily killing step-children. 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. […]

Let us take Maynard Smith’s method of analysing aggressive contests, and apply it to sex. This idea of trying to find an evolutionarily stable mix of strategies within one sex, balanced by an evolutionarily stable mix of strategies in the other sex, has now been taken further by Maynard Smith himself and, independently but in a similar direction, by Alan Grafen and Richard Sibly. Grafen and Sibly’s paper is the more technically advanced, Maynard Smith’s the easier to explain in words. Briefly, he begins by considering two strategies, Guard and Desert, which can be adopted by either sex. As in my ‘coy/fast and faithful/philanderer’ model, the interesting question is, what combinations of strategies among males are stable against what combinations of strategies among females? The answer depends upon our assumption about the particular economic circumstances of the species. Interestingly, though, however much we vary the economic assumptions, we don’t have a whole continuum of quantitatively varying stable outcomes. The model tends to home in on one of only four stable outcomes. The four outcomes are named after animal species that exemplify them. There is the Duck (male deserts, female guards), the Stickleback (female deserts, male guards), the Fruit-fly (both desert) and the Gibbon (both guard). And here is something even more interesting. Remember from Chapter 5 that ESS models can settle at either of two outcomes, both equally stable? Well, that is true of this Maynard Smith model, too. What is especially interesting is that particular pairs, as opposed to other pairs, of these outcomes are jointly stable under the same economic circumstances. For instance, under one range of circumstances, both Duck and Stickleback are stable. Which of the two actually arises depends upon luck or, more precisely, upon accidents of evolutionary history—initial conditions. Under another range of circumstances, both Gibbon and Fruit-fly are stable. Again, it is historical accident that determines which of the two occurs in any given species. But there are no circumstances in which Gibbon and Duck are jointly stable, no circumstances in which Duck and Fruit-fly are jointly stable. This ‘stablemate’ (to coin a double pun) analysis of congenial and uncongenial combinations of ESSs has interesting consequences for our reconstructions of evolutionary history. For instance, it leads us to expect that certain kinds of transitions between mating systems in evolutionary history will be probable, others improbable. Maynard Smith explores these historical networks in a brief survey of mating patterns throughout the animal kingdom, ending with the memorable rhetorical question: ‘Why don’t male mammals lactate?’ […]

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.

cases of paternal devotion . . . common among fish. Why?

Tamsin Carlisle’s undergraduate hypothesis about fish has now been tested comparatively by Mark Ridley, in the course of an exhaustive review of paternal care in the entire animal kingdom. His paper is an astonishing tour de force which, like Carlisle’s hypothesis itself, also began as an undergraduate essay written for me. Unfortunately he did not find in favour of the hypothesis.

It was Hamilton who brilliantly realized that, at least in the ants, bees, and wasps, the workers may actually be more closely related to the brood than the queen herself is! This led him, and later Trivers and Hare, on to one of the most spectacular triumphs of the selfish gene theory. The reasoning goes like this. Insects of the group known as the Hymenoptera, including ants, bees, and wasps, have a very odd system of sex determination. Termites do not belong to this group and they do not share the same peculiarity. A hymenopteran nest typically has only one mature queen. She made one mating flight when young and stored up the sperms for the rest of her long life—ten years or even longer. She rations the sperms out to her eggs over the years, allowing the eggs to be fertilized as they pass out through her tubes. But not all the eggs are fertilized. The unfertilized ones develop into males. A male therefore has no father, and all the cells of his body contain just a single set of chromosomes (all obtained from his mother) instead of a double set (one from the father and one from the mother) as in ourselves. In terms of the analogy of Chapter 3, a male hymenopteran has only one copy of each ‘volume’ in each of his cells, instead of the usual two. A female hymenopteran, on the other hand, is normal in that she does have a father, and she has the usual double set of chromosomes in each of her body cells. Whether a female develops into a worker or a queen depends not on her genes but on how she is brought up. That is to say, each female has a complete set of queen-making genes, and a complete set of worker-making genes (or, rather, sets of genes for making each specialized caste of worker, soldier, etc.). Which set of genes is ‘turned on’ depends on how the female is reared, in particular on the food she receives. Although there are many complications, this is essentially how things are. We do not know why this extraordinary system of sexual reproduction evolved. No doubt there were good reasons, but for the moment we must just treat it as a curious fact about the Hymenoptera. Whatever the original reason for the oddity, it plays havoc with Chapter 6’s neat rules for calculating relatedness. It means that the sperms of a single male, instead of all being different as they are in ourselves, are all exactly the same. A male has only a single set of genes in each of his body cells, not a double set. Every sperm must therefore receive the full set of genes rather than a 50 per cent sample, and all sperms from a given male are therefore identical. Let us now try to calculate the relatedness between a mother and son. If a male is known to possess a gene A, what are the chances that his mother shares it? The answer must be 100 per cent, since the male had no father and obtained all his genes from his mother. But now suppose a queen is known to have the gene B. The chance that her son shares the gene is only 50 per cent, since he contains only half her genes. This sounds like a contradiction, but it is not. A male gets all his genes from his mother, but a mother only gives half her genes to her son. The solution to the apparent paradox lies in the fact that a male has only half the usual number of genes. There is no point in puzzling over whether the ‘true’ index of relatedness is ½ or I. The index is only a man-made measure, and if it leads to difficulties in particular cases, we may have to abandon it and go back to first principles. From the point of view of a gene A in the body of a queen, the chance that the gene is shared by a son is ½, just as it is for a daughter. From a queen’s point of view therefore, her offspring, of either sex, are as closely related to her as human children are to their mother. Things start to get intriguing when we come to sisters. Full sisters not only share the same father: the two sperms that conceived them were identical in every gene. The sisters are therefore equivalent to identical twins as far as their paternal genes are concerned. If one female has a gene A, she must have got it from either her father or her mother. If she got it from her mother then there is a 50 per cent chance that her sister shares it. But if she got it from her father, the chances are 100 per cent that her sister shares it. Therefore the relatedness between hymenopteran full sisters is not as it would be for normal sexual animals, but . It follows that a hymenopteran female is more closely related to her full sisters than she is to her offspring of either sex.* As Hamilton realized (though he did not put it in quite the same way) this might well predispose a female to farm her own mother as an efficient sister-making machine. A gene for vicariously making sisters replicates itself more rapidly than a gene for making offspring directly. Hence worker sterility evolved. It is presumably no accident that true sociality, with worker sterility, seems to have evolved no fewer than eleven times independently in the Hymenoptera and only once in the whole of the rest of the animal kingdom, namely in the termites. However, there is a catch. If the workers are successfully to farm their mother as a sister-producing machine, they must somehow curb her natural tendency to give them an equal number of little brothers as well. From the point of view of a worker, the chance of any one brother containing a particular one of her genes is only . Therefore, if the queen were allowed to produce male and female reproductive offspring in equal proportions, the farm would not show a profit as far as the workers are concerned. They would not be maximizing the propagation of their precious genes. Trivers and Hare realized that the workers must try to bias the sex ratio in favour of females. They took the Fisher calculations on optimal sex ratios (which we looked at in the previous chapter) and re-worked them for the special case of the Hymenoptera. It turned out that the stable ratio of investment for a mother is, as usual, 1: 1. But the stable ratio for a sister is 3: 1 in favour of sisters rather than brothers. If you are a hymenopteran female, the most efficient way for you to propagate your genes is to refrain from breeding yourself, and to make your mother provide you with reproductive sisters and brothers in the ratio 3:1. But if you must have offspring of your own, you can benefit your genes best by having reproductive sons and daughters in equal proportions. As we have seen, the difference between queens and workers is not a genetic one. As far as her genes are concerned, an embryo female might be destined to become either a worker, who ‘wants’ a 3: 1 sex ratio, or a queen, who ‘wants’ a 1: 1 ratio. So what does this ‘wanting’ mean? It means that a gene that finds itself in a queen’s body can propagate itself best if that body invests equally in reproductive sons and daughters. But the same gene finding itself in a worker’s body can propagate itself best by making the mother of that body have more daughters than sons. There is no real paradox here. A gene must take best advantage of the levers of power that happen to be at its disposal. If it finds itself in a position to influence the development of a body that is destined to turn into a queen, its optimal strategy to exploit that control is one thing. If it finds itself in a position to influence the way a worker’s body develops, its optimal strategy to exploit that power is different. This means there is a conflict of interests down on the farm. The queen is ‘trying’ to invest equally in males and females. The workers are trying to shift the ratio of reproductives in the direction of three females to every one male. If we are right to picture the workers as the farmers and the queen as their brood mare, presumably the workers will be successful in achieving their 3: 1 ratio. If not, if the queen really lives up to her name and the workers are her slaves and the obedient tenders of the royal nurseries, then we should expect the 1: 1 ratio which the queen ‘prefers’ to prevail. Who wins in this special case of a battle of the generations? This is a matter that can be put to the test and that is what Trivers and Hare did, using a large number of species of ants. The sex ratio that is of interest is the ratio of male to female reproductives. These are the large winged forms which emerge from the ants’ nest in periodic bursts for mating flights, after which the young queens may try to found new colonies. It is these winged forms that have to be counted to obtain an estimate of the sex ratio. Now the male and female reproductives are, in many species, very unequal in size. This complicates things since, as we saw in the previous chapter, the Fisher calculations about optimal sex ratio strictly apply, not to numbers of males and females, but to quantity of investment in males and females. Trivers and Hare made allowance for this by weighing them. They took 20 species of ant and estimated the sex ratio in terms of investment in reproductives. They found a rather convincingly close fit to the 3: 1 female to male ratio predicted by the theory that the workers are running the show for their own benefit.* It seems then that in the ants studied, the conflict of interests is ‘won’ by the workers. This is not too surprising since worker bodies, being the guardians of the nurseries, have more power in practical terms than queen bodies. Genes trying to manipulate the world through queen bodies are outmanœuvred by genes manipulating the world through worker bodies. It is interesting to look around for some special circumstances in which we might expect queens to have more practical power than workers. Trivers and Hare realized that there was just such a circumstance which could be used as a critical test of the theory. This arises from the fact that there are some species of ant that take slaves. The workers of a slave-making species either do no ordinary work at all or are rather bad at it. What they are good at is going on slaving raids. True warfare in which large rival armies fight to the death is known only in man and in social insects. In many species of ants the specialized caste of workers known as soldiers have formidable fighting jaws, and devote their time to fighting for the colony against other ant armies. Slaving raids are just a particular kind of war effort. The slavers mount an attack on a nest of ants belonging to a different species, attempt to kill the defending workers or soldiers, and carry off the unhatched young. These young ones hatch out in the nest of their captors. They do not ‘realize’ that they are slaves and they set to work following their built-in nervous programs, doing all the duties that they would normally perform in their own nest. The slave-making workers or soldiers go on further slaving expeditions while the slaves stay at home and get on with the everyday business of running an ants’ nest, cleaning, foraging, and caring for the brood. The slaves are, of course, blissfully ignorant of the fact that they are unrelated to the queen and to the brood that they are tending. Unwittingly they are rearing new platoons of slave-makers. No doubt natural selection, acting on the genes of the slave species, tends to favour anti-slavery adaptations. However, these are evidently not fully effective because slavery is a wide spread phenomenon. The consequence of slavery that is interesting from our present point of view is this. The queen of the slave-making species is now in a position to bend the sex ratio in the direction she ‘prefers’. This is because her own true-born children, the slavers, no longer hold the practical power in the nurseries. This power is now held by the slaves. The slaves ‘think’ they are looking after their own siblings and they are presumably doing whatever would be appropriate in their own nests to achieve their desired 3: 1 bias in favour of sisters. But the queen of the slave-making species is able to get away with countermeasures and there is no selection operating on the slaves to neutralize these counter-measures, since the slaves are totally unrelated to the brood. For example, suppose that in any ant species, queens ‘attempt’ to disguise male eggs by making them smell like female ones. Natural selection will normally favour any tendency by workers to ‘see through’ the disguise. We may picture an evolutionary battle in which queens continually ‘change the code’, and workers ‘break the code’. The war will be won by whoever manages to get more of her genes into the next generation, via the bodies of the reproductives. This will normally be the workers, as we have seen. But when the queen of a slave-making species changes the code, the slave workers cannot evolve any ability to break the code. This is because any gene in a slave worker ‘for breaking the code’ is not represented in the body of any reproductive individual, and so is not passed on. The reproductives all belong to the slave-making species, and are kin to the queen but not to the slaves. If the genes of the slaves find their way into any reproductives at all, it will be into the reproductives that emerge from the original nest from which they were kidnapped. The slave workers will, if anything, be busy breaking the wrong code! Therefore, queens of a slave-making species can get away with changing their code freely, without there being any danger that genes for breaking the code will be propagated into the next generation. The upshot of this involved argument is that we should expect in slave-making species that the ratio of investment in reproductives of the two sexes should approach 1: 1 rather than 3:1. For once, the queen will have it all her own way. This is just what Trivers and Hare found, although they only looked at two slave-making species. I must stress that I have told the story in an idealized way. Real life is not so neat and tidy. For instance, the most familiar social insect species of all, the honey bee, seems to do entirely the ‘wrong’ thing. There is a large surplus of investment in males over queens—something that does not appear to make sense from either the workers’ or the mother queen’s point of view.

Alan Grafen pointed out to me another and more worrying problem with the account of hymenopteran sex ratios given in the first edition of this book. I have explained his point in The Extended Phenotype (pp. 75–6). Here is a brief extract:

The potential worker is still indifferent between rearing siblings and rearing offspring at any conceivable population sex ratio. Thus suppose the population sex ratio is female-biased, even suppose it conforms to Trivers and Hare’s predicted 3:1. Since the worker is more closely related to her sister than to her brother or her offspring of either sex, it might seem that she would ‘prefer’ to rear siblings over offspring given such a female-biased sex ratio: is she not gaining mostly valuable sisters (plus only a few relatively worthless brothers) when she opts for siblings? But this reasoning neglects the relatively great reproductive value of males in such a population as a consequence of their rarity. The worker may not be closely related to each of her brothers, but if males are rare in the population as a whole each one of those brothers is correspondingly highly likely to be an ancestor of future generations.

Richard Dawkins, The Selfish Gene, 30th Anniversary Edition, 2006

Footnotes (1989 edition) are doubly indented.