Whether 99 per cent is an exaggeration or not, Washburn is certainly right that any two random members of a species share the great majority of their genes. What, then, are we talking about when we speak of the coefficient of relatedness r between, say, siblings as being 50 per cent? We must answer this question first before getting down to the error itself.
The unqualified statement that parents and offspring share 50 per cent of their genes is, as Washburn rightly says, false. It can be made true by means of a qualification. A lazy way of qualifying it is to announce that we are only talking about rare genes; if I have a gene that is very rare in the population as a whole, the probability that my child or my brother has it is about 50 per cent. This is lazy because it evades the important fact that Hamilton’s reasoning applies at all frequencies of the gene in question; it is an error (see Misunderstanding 6) to suppose that the theory only works for rare genes. Hamilton’s own way of qualifying the statement is different. It is to add the phrase ‘identical by descent’. Siblings may share 99 per cent of their genes altogether, but only 50 per cent of their genes are identical by descent, that is, are descended from the same copy of the gene in their most recent common ancestor.
So, we have identified two ways of explaining the meaning of r, the coefficient of relatedness: the ‘rare gene’ way and the ‘identical by descent’ way.*10 Neither of these, however, shows us how to escape from Washburn’s paradox. Why is it not the case that natural selection will favour universal altruism, since most genes are universally shared in a species?
Let there be two strategies, Universal Altruist U, and Kin Altruist K. U individuals care for any member of the species indiscriminately. K individuals care for close kin only. In both cases, the caring behaviour costs the altruist something in terms of his personal survival chances. Suppose we grant Washburn’s assumption that U behaviour ‘is based on the shared 99 per cent of genes’. In other words, virtually the entire population are universal altruists, and a tiny minority of mutants or immigrants are kin altruists. Superficially, the U gene appears to be caring for copies of itself, since the beneficiaries of its indiscriminate altruism are almost bound to contain the same gene. But is it evolutionarily stable against invasion by initially rare K genes?*11
No, it is not. Every time a rare K individual behaves altruistically, it is especially likely to benefit another K individual rather than a U individual. U individuals, on the other hand, give out altruism to K individuals and U individuals indiscriminately, since the defining characteristic of U behaviour is that it is indiscriminate. Therefore K genes are bound to spread through the population at the expense of U genes. Universal altruism is not evolutionarily stable against kin altruism. Even if we assume it to be initially common, it will not remain common. This leads directly into the next, complementary, misunderstanding.
Misunderstanding 6: ‘Kin selection only works for rare genes’
The logical outcome of the statement that, say, sibling altruism is favoured by natural selection, is that the relevant genes will spread to fixation.*12 Virtually all individuals in the population will be sibling altruists. Therefore, if they did but know it, they would benefit the gene for sibling altruism just as much by caring for a random member of the species as by caring for a sibling! So it might seem that genes for exclusive kin altruism are favoured only when rare.
To put it this way is to expect animals, even genes, to play God. Natural selection is more mechanical than that.*13 The kin altruism gene does not program individuals to take intelligent action on its behalf; it specifies a simple behavioural rule of thumb such as ‘feed squawking gapes in the nest in which you live’. It is this unconscious rule that will become universal when the gene becomes universal.
As in the case of the previous fallacy, we can use the language of evolutionarily stable strategies. We now ask whether kin altruism, K, is stable against invasion by universal altruism, U. That is, we assume that kin altruism has become common and ask whether mutant universal altruist genes will invade. The answer is no, for the same reason as before. The rare universal altruists care for the rival K allele indiscriminately with copies of their own U allele. The K allele, on the contrary, is especially unlikely to care for copies of its rival.
We have shown, therefore, that kin altruism is stable against invasion by universal altruism, but that universal altruism is not stable against invasion by kin altruism. This is the nearest I can get to a verbal explanation of Hamilton’s mathematical argument that altruism to close relatives is favoured over universal altruism at all frequencies of the genes concerned. Although it lacks the mathematical precision of Hamilton’s own presentation, it should at least suffice to remove these two common qualitative misunderstandings.
Misunderstanding 7: ‘Altruism is necessarily expected between members of an identical clone’
There are races of parthenogenetic*14 lizards the members of which appear to be identical descendants, in each case, of a single mutant. The coefficient of relatedness between individuals within such a clone is 1. A naive application of rote-learned kin selection theory might therefore predict great feats of altruism between all members of the race. Like the previous one, this fallacy is tantamount to a belief that genes are god-like.
Genes for kin altruism spread because they are especially likely to help copies of themselves rather than of their alleles. But the members of a lizard clone all contain the genes of their original founding matriarch. She was part of an ordinary sexual population, and there is no reason to suppose that she had any special genes for altruism. When she founded her asexual clone, her existing genome was ‘frozen’: a genome that had been shaped by whatever selection pressures had been at work before the clonal mutation.
Should any new mutation for more indiscriminate altruism arise within the clone, the possessors of it would be, by definition, members of a new clone. Evolution could therefore, in theory, now occur by inter-clonal selection. But the new mutation would have to work via a new rule of thumb. If the new rule of thumb is so indiscriminate that both sub-clones benefit, the altruistic sub-clone is bound to decrease, since it is paying the cost of the altruism. We could imagine a new rule of thumb that initially achieved discrimination in favour of the altruistic sub-clone. But this would have to be something like an ordinary ‘close-kin’ altruism rule of thumb (e.g. ‘care for occupants of your own nest’). Then if the sub-clone possessing this rule of thumb did indeed spread at the expense of the selfish sub-clone, what would we eventually see? Simply a race of lizards in which each one cared for occupants of her own nest: not clone-wide altruism but ordinary ‘close-kin’ altruism. (Pedants please refrain from commenting that lizards don’t have nests!)
I hasten to add, however, that there are other circumstances in which clonal reproduction is expected to lead to special altruism. Nine-banded armadillos have become a favourite talking point, because they reproduce sexually but each litter consists of four identical quadruplets. Here within-clone altruism is indeed expected, because genes are reassorted sexually in each generation in the usual way. This means that any gene for clonal altruism is likely to be shared by all members of some clones and no members of rival clones.
There is, so far, no good evidence for or against the predicted within-clone altruism in armadillos. However, some intriguing evidence in a comparable case has been reported by Aoki. In the Japanese aphid Colophina clematis, sisterhoods of asexually produced females consist of two types of individuals. Type A females are normal plant-sucking aphids. Type B females do not progress beyond 1st instar*15 and never reproduce. They have an abnormally short rostrum which is ill-adapted to sucking plants, and enlarged ‘pseudoscorpion-like’ prothoracic and mesothoracic legs. Aoki showed that Type B females attack large insects and kill them. He speculated that they constitute a sterile ‘soldier caste’ who protect their reproductive sisters against predators. It is not known how the ‘soldiers’ feed. Aoki doubts that their fighting mouthparts are capable of absorbing sap. H
e does not suggest that they are fed by their Type A sisters, but that fascinating possibility is presumably open. He reports indications of similar soldier castes in other aphid genera.
There is a nice irony in Aoki’s discussion, brought to my attention by R. L. Trivers. ‘It may be concluded from [Hamilton’s] theory that true sociality should occur more frequently in groups with haplodiploidy than in those without it…I do not know how many occurrences of true sociality among animals without haplodiploidy would be sufficient to refute his theory. The existence of soldiers in aphids should take part in one of the gravest problems against his theory, however.’*16
This error is most instructive. Colophina clematis, like other aphids, have winged sexually reproducing dispersal phases interspersed with viviparous parthenogenetic generations. The ‘soldiers’ and the Type A individuals whom they seem to protect are wingless, and are almost certainly members of the same clone. The regular intervention of winged sexual generations ensures that genes for facultatively developing into a soldier, and alleles for not doing so, would be shuffled throughout the population. Some clones would therefore have such genes while rival clones would not. Conditions, in fact, are quite different from those of the lizards, and are ideal for the evolution of sterile castes. The soldiers and their reproductive clone mates are best regarded as parts of the same extended body. If a soldier aphid altruistically sacrifices her own reproduction, then so does my big toe. In almost exactly the same sense!
Misunderstanding 10: ‘Individuals should tend to inbreed, simply because this brings extra close relatives into the world’
I have to be careful here, because there is a correct line of reasoning that sounds very like the error. Moreover, there may be other selection pressures for and against inbreeding, but these have nothing to do with the present argument: the proponent of the misconception is assumed to have covered himself with an ‘other things being equal’.
The reasoning I wish to criticize runs as follows. Assume a monogamous mating system. A female who mates with a random male brings into the world a child related to her by r = ½. If only she had mated with her brother she would have brought into the world a ‘super-child’ with an effective coefficient of relatedness of ¾. Therefore genes for inbreeding are propagated at the expense of genes for outbreeding, having a greater probability of getting into each child born.
The error is a simple one. If the individual refrains from mating with her brother, he is free to mate with some other female. So an outbreeding female gains a nephew/niece (r = ¼) plus a normal child of her own (r = ½) to match the single super-child of the incestuous female (effective r = ¾). It is important to note that the refutation of the error assumes the equivalent of monogamy. If the species is, say, polygynous*17 with high variance in male reproductive success and a large bachelor population, things can be very different. It is now no longer true that a female, by mating with her brother, deprives him of the chance to mate with someone else. Most probably, the free mating his sister gives him is the only mating he will get. The female therefore does not deprive herself of an independent niece/nephew by mating incestuously, and she does bring into the world a child who is a super-child from her own genetic point of view. There may, then, be selection pressures in favour of incest, but the heading to this section is, as a general statement, incorrect.
Misunderstanding 12: ‘An animal is expected to dole out to each relative an amount of altruism proportional to the coefficient of relatedness’
As S. Altmann has pointed out, I perpetrated this error when I wrote that ‘second cousins should tend to receive one-sixteenth as much altruism as offspring or siblings’.*18 To oversimplify Altmann’s argument, suppose I have a cake that I am going to give to my relatives, how should I divide it? The fallacy under discussion amounts to cutting the cake in such a way that each relative gets a slice whose size is proportional to his coefficient of relatedness to me. Really, of course, there is better reason to give the entire cake to the closest relative available and none to any of the others.
Suppose each mouthful of cake was equally valuable, translated into offspring flesh in simple pro-rata fashion. Then clearly an individual should prefer that his whole cake should be translated into closely related flesh than distantly related flesh. Of course this simple pro-rata assumption would almost certainly be false in real cases. However, quite elaborate assumptions about diminishing returns would have to be made before we could sensibly predict that the cake should be divided in exact proportion to coefficients of relatedness. Therefore, although my statement quoted above could under special circumstances be true, as a generalization it is properly regarded as fallacious. Of course I didn’t really mean it anyway!
Apology
If the foregoing pages seem destructive or negative in tone, the very opposite was my intention. The art of explaining difficult material consists, in part, of anticipating the reader’s difficulties and forestalling them. Systematically exposing common misunderstandings can therefore be a positively constructive exercise. I believe I understand kin selection better for having met these twelve errors, for having, in many cases, fallen into the trap myself and struggled painfully out the other side.
* * *
*1 The theory of kin selection – natural selection favours genes for helping relatives because they are statistically likely to be present in the relatives helped – was developed by W. D. Hamilton, who later became my Oxford colleague and friend. It was one of the central themes of my first book, The Selfish Gene. Having been largely neglected for its first decade after Hamilton’s important papers of 1964, the theory of kin selection suddenly became much discussed in the mid-1970s by biologists and the wider world. Kin selection’s popularity spawned a rich plethora of misunderstandings, some of the more bizarre ones being perpetrated by distinguished social scientists who – dare one suggest – may have felt threatened by this sudden incursion into what they thought was their field. This upsurge of wayward commentary prompted me to collect twelve of these misunderstandings and refute them in an article published (in English) in the leading German journal of animal behaviour, the Zeitschrift für Tierpsychologie. As usual in a scientific paper, there were many references to the literature. These have been omitted here. I have also cut three of the misunderstandings, numbers 8, 9 and 11. Although they are important, they concern technicalities which could only be made clear by providing an excess of space-filling background information.
*2 Today my consciousness has been raised to the point where I’d say ‘with her ear to the ground’. Not ‘his or her’, which sounds obtrusively clumsy to my ear. I prefer the convention by which authors signal courteous respect for the sex opposite to their own by favouring the appropriate pronouns. Ethology is the biological study of animal behaviour. Nowadays I could equally well have said ‘sensitive sociobiologist’, ‘sensitive behavioural ecologist’ or ‘sensitive evolutionary psychologist’ with her ear to the ground.
*3 ‘Hamilton’s Rule’ succinctly sums up his theory. A gene for altruism will spread through the gene pool if r B >C, i.e. if the cost C to the altruist is outweighed by the benefit B to the recipient multiplied by a fraction r, representing the closeness of genetic relationship between them. The reason parental care is commoner than care of full siblings is that, although r is the same for both relationships (0.5), the B and C terms in practice favour parental care.
*4 Unfortunately both these improvements have been reversed by Wilson in more recent publications, including his book The Social Conquest of Earth, in ways that suggest to me that he never really understood kin selection in the first place.
*5 Hamilton gave ‘inclusive fitness’ a more precise mathematical definition which can be rendered, somewhat lengthily, into words, but he approved my informal definition: ‘Inclusive fitness is that quantity which an individual will appear to be maximizing when what is really being maximized is the survival of its genes.’
*6 Many genes have more than one effect, often a
pparently unconnected with each other, and the phenomenon is called pleiotropy.
*7 The Green Beard Effect is an unrealistic hypothetical, a parable. What is realistic – and this is the point of the parable – is that kinship acts as a kind of statistical green beard. An animal with a genetic propensity to care for full siblings, say, has a 50 per cent chance that it is caring for copies of itself. Brotherhood is a label like a green beard. We do not expect animals to be cognitively aware of brotherhood. In practice the label is likely to be something like ‘he who sits in the same nest as you’.
*8 Marshall Sahlins is a distinguished American anthropologist. Some other anthropologists have taken the trouble to learn some biology. To be fair, I expect I would exhibit similar ignorance and lack of understanding, were I to wade into the field of anthropology. But I do not so wade.
*9 ‘Alleles’ are alternative forms of a gene which vie for a particular slot or ‘locus’ on a chromosome. In sexually reproducing creatures, natural selection can be seen as competition between alleles in the gene pool for that slot. The weapons of their competition are normally the ‘phenotypic’ effects that they have on bodies.
*10 See also the footnote on this page.
*11 ‘Evolutionarily stable strategy’ or ESS is John Maynard Smith’s phrase, and it represents a powerful way of thinking about evolution, one of which I made extensive use in The Selfish Gene. A ‘strategy’ is a piece of unconscious behavioural ‘clockwork’ such as ‘drop food into squawking gapes that you see in your nest’. An ESS is a strategy such that, when a majority of the population adopts it, it cannot be bettered by an alternative strategy. If it can be bettered, it is ‘unstable’. A population dominated by an unstable strategy will be ‘invaded’ by the superior alternative strategy. ESS reasoning commonly starts with a statement such as: ‘Imagine a strategy P, such that all members of the population are doing P. Now imagine that a new strategy, Q, were to arise by mutation; would natural selection cause Q to “invade”?’ That is what we are doing in our reasoning about the strategies U and K.
Science in the Soul Page 19
