* * *
*1 Ernst Mayr was an illustrious German-American biologist, one of the founding fathers of the neo-Darwinian synthesis of the 1930s and 1940s. He could indeed be called the Grand Old Man of the synthesis, not least because he did live to be very old. He was a hundred when I met him and he was active and alert to the end. Among the many honours bestowed on him and the many publications devoted to his celebration was a Festschrift volume of the journal Ludus Vitalis, edited by the distinguished Spanish-American geneticist Francisco Ayala, to which I was invited to contribute the paper which appears here (slightly abbreviated). I dedicated it, ‘with the very deepest respect, to Professor Ernst Mayr FRS, Hon. D.Sc. (Oxford) on the occasion of his hundredth birthday’.
*2 See the preceding essay in this collection, ‘Universal Darwinism’.
*3 Which makes it all the more surprising that Aristotle, no fool, could seriously entertain it. Aristotle is one of many highly intelligent thinkers who, one might suppose, could have worked out the principle of evolution by natural selection, but didn’t. Why not? Evolution by natural selection is the kind of idea, you might think, that could occur to a great thinker and naturalist in any century. Unlike Newton’s physics, it’s hard to see why it needed two millennia of shoulders to stand on. However, it clearly did, so my intuition must be just plain wrong.
*4 Such mysticism reached its apogee in early versions of James Lovelock’s Gaia hypothesis. In later versions Lovelock himself sought to disavow the mysticism, but it was still going strong at a conference where John Maynard Smith met a prominent devotee of ‘Ecology’ in the political rather than the scientific sense of the word. Somebody mentioned the theory that a large meteorite had struck Earth, thereby killing the dinosaurs. ‘Of course not,’ declared the fervent ‘Ecologist’, by Maynard Smith’s account; ‘Gaia would not have permitted it.’
*5 The ecologist Lawrence Slobodkin, who introduced the phrase, was later stung into indignant denial of the charge of group selectionism (American Naturalist, vol. 108, 1974). He may be right that a proper Darwinian defence of ‘prudent predators’ can – at a bit of a stretch – be mounted. But the phrase was ill-chosen. It begs to be interpreted along the lines of the Great Ecological Temptation – to forget the level at which natural selection actually works to produce individual adaptations, and think in terms of benefit to the group or even the community.
*6 It provoked J. B. S. Haldane’s spirited ‘Defence of beanbag genetics’. Beanbag genetics, in this context, means the quantitative treatment of changes in gene frequency in populations, treating genes as particulate Mendelian entities.
Twelve misunderstandings of kin selection*1
Introduction
KIN SELECTION HAS become a bandwagon, and when bandwagons start to roll attitudes sometimes polarize. The rush to jump on provokes a healthy reaction. So it is that today the sensitive ethologist with his*2 ear to the ground detects a murmuring of sceptical growls, rising to an occasional crescendo of smug baying when one of the early triumphs of the theory encounters new problems. Such polarization is a pity. In this case it is exacerbated by a notable series of misunderstandings, both on and off the kin selection bandwagon. Many of these misunderstandings arise from secondary attempts at explaining Hamilton’s ideas rather than from his original mathematical formulation. As one who has fallen for some of them in my time and met all of them frequently, I would like to try the difficult exercise of explaining in non-mathematical language twelve of the commonest misunderstandings of kin selection. The twelve by no means exhaust the supply. Alan Grafen, for instance, has published good exposés of two other, rather more subtle ones. The twelve sections can be read in any order.
Misunderstanding 1: ‘Kin selection is a special, complex kind of natural selection, to be invoked only when “individual selection” proves inadequate’
This one logical error, on its own, is responsible for a large part of the sceptical backlash that I mentioned. It results from a confusion between historical precedence and theoretical parsimony: ‘Kin selection is a recent addition to our theoretical armoury; for many purposes we got along quite well without it for years; therefore we should turn to it only when good old-fashioned “individual selection” fails us.’
Note that good old-fashioned individual selection has always included parental care as an obvious consequence of selection for individual fitness. What the theory of kin selection has added is that parental care is only a special case of caring for close relatives. If we look in detail at the genetical basis of natural selection, we see that ‘individual selection’ is anything but parsimonious, while kin selection is a simple and inevitable consequence of the differential gene survival that, fundamentally, is natural selection. Caring for close relatives at the expense of distant relatives is predicted from the fact that close relatives have a high chance of propagating the gene or genes ‘for’ such caring: the gene cares for copies of itself. Caring for oneself and one’s own children but not equally close collateral relatives is hard to predict by any simple genetic model. We have to invoke additional factors, such as the assumption that offspring are easier to identify or easier to help than collateral relatives. These additional factors are perfectly plausible but they have to be added to the basic theory.
It happens to be true that most animals care for offspring more than they care for siblings, and it is certainly true that evolutionary theorists understood parental care before they understood sibling care. But neither of these two facts implies that the general theory of kin selection is unparsimonious. If you accept the genetical theory of natural selection, as all serious biologists now do, then you must accept the principles of kin selection. Rational scepticism is limited to beliefs (perfectly sensible ones) that in practice the selection pressure in favour of caring for relatives other than offspring is unlikely to have noticeable evolutionary consequences.*3
Misunderstanding 1 has perhaps been unwittingly encouraged by an influential definition of kin selection propagated by Edward O. Wilson: ‘the selection of genes due to one or more individuals favoring or disfavoring the survival and reproduction of relatives (other than offspring) who possess the same genes by common descent’. I am glad to see that Wilson has omitted the phrase ‘other than offspring’ in his more recent definition, in favour of the following: ‘Although kin are defined so as to include offspring, the term kin selection is ordinarily used only if at least some other relatives, such as brothers, sisters, or parents, are also affected.’ This is undeniably true, but I still think it is regrettable. Why should we treat parental care as special, just because for a long time it was the only kind of kin-selected altruism we understood? We do not separate Neptune and Uranus off from the rest of the planets simply because for centuries we did not know of their existence. We call them all planets because they are all the same kind of thing.
At the end of his 1975 definition, Wilson added that kin selection was ‘one of the extreme forms of group selection’. This, too, has happily been deleted from his 1978 definition.*4 It is the second of my twelve misunderstandings.
Misunderstanding 2: ‘Kin selection is a form of group selection’
Group selection is the differential survival or extinction of whole groups of organisms. It happens that organisms sometimes go around in family groups, and it follows that differential group extinction could turn out to be effectively equivalent to family selection or ‘kin group selection’. But this has nothing to do with the essence of Hamilton’s basic theory: those genes are selected that tend to make individuals discriminate in favour of other individuals who are especially likely to contain copies of the same genes. The population does not need to be divided up into family groups in order for this to happen, and it is certainly not necessary that whole families should go extinct or survive as units.
Animals cannot, of course, be expected to know, in a cognitive sense, who their relatives are (see Misunderstanding 3), and in practice the behaviour that is favoured by natural sele
ction will be equivalent to a rough rule of thumb such as ‘share food with anything that moves, in the nest in which you are sitting’. If families happen to go around in groups, this fact provides a useful rule of thumb for kin selection: ‘Care for any individual you often see.’ But note once again that this has nothing to do with true group selection: differential survival and extinction of whole groups do not enter into the reasoning. The rule of thumb works if there is any ‘viscosity’ in the population such that individuals are statistically likely to encounter relatives; there is no need for families to go about in discrete groups.
Hamilton is perhaps right to blame the phrase ‘kin selection’ itself for some misunderstanding, ironically since it was coined (by Maynard Smith) with the laudable purpose of emphasizing its distinctness from group selection. Hamilton himself does not use the phrase, preferring to stress the relevance of his central concept of inclusive fitness*5 to any kind of genetically non-random altruism, whether concerned with kin-relatedness or not. For instance, suppose that within a species there is genetic variation in habitat choice. Suppose further that one of the genes contributing to this variation has the pleiotropic*6 effect of making individuals share food with others whom they encounter. Because of the pleiotropic effect on habitat choice, this altruistic gene is effectively discriminating in favour of copies of itself, since individuals possessing it are especially likely to congregate in the same habitat and therefore meet each other. They do not have to be close kin.
Any way in which an altruistic gene can ‘recognize’ copies of itself in other individuals could form the basis for a similar model. The principle is reduced to its bare essentials in the improbable but instructive ‘Green Beard Effect’: selection would theoretically favour a gene that pleiotropically caused individuals to develop a green beard and also a tendency to be altruistic to green-bearded individuals. Again there is no need for the individuals to be kin.*7
Misunderstanding 3: ‘The theory of kin selection demands formidable feats of cognitive reasoning by animals’
In a much-quoted ‘anthropological critique of sociobiology’, Sahlins*8 says the following:
In passing it needs to be remarked that the epistemological problems presented by a lack of linguistic support for calculating r, coefficients of relationship, amount to a serious defect in the theory of kin selection. Fractions are of very rare occurrence in the world’s languages, appearing in Indo-European and in the archaic civilizations of the Near and Far East, but they are generally lacking among the so-called primitive peoples. Hunters and gatherers generally do not have counting systems beyond one, two and three. I refrain from comment on the even greater problem of how animals are supposed to figure out how that r [ego, first cousins] = 1/8. The failure of sociobiologists to address this problem introduces a considerable mysticism in their theory.
A pity, for Sahlins, that he succumbed to the temptation to ‘refrain from comment’ on how ‘animals are supposed to figure out’ r. The very absurdity of the idea he tried to ridicule should have set mental alarm bells ringing. A snail shell is an exquisite logarithmic spiral, but where does the snail keep its log tables; how indeed does it read them, since the lens in its eye lacks ‘linguistic support’ for calculating µ, the coefficient of refraction? How do green plants ‘figure out’ the formula of chlorophyll? Enough, let us be constructive.
Natural selection chooses genes rather than their alleles,*9 because of those genes’ phenotypic effects. In the case of behaviour, the genes presumably influence the state of the nervous system, which in turn influences the behaviour. Whether it is behaviour, physiology or anatomy, a complex phenotype may require sophisticated mathematical description if we are to understand it. This does not, of course, mean that the animals themselves have to be mathematicians. Unconscious ‘rules of thumb’ of the kind already mentioned will be selected. For a spider to build a web, rules of thumb are required that are probably more sophisticated than any that kin-selection theorists have postulated. If spider webs did not exist, anybody who postulated them might well provoke scornful scepticism. But they do exist; we have all seen them, and nobody wonders how spiders ‘figure out’ the designs.
The machinery that automatically and unconsciously builds webs must have evolved by natural selection. Natural selection means the differential survival of alleles in gene pools. There must, therefore, have been genetic variation in the tendency to build webs. Similarly, to talk about the evolution of altruism by kin selection we have to postulate genetic variation in altruism. In this sense we have to postulate alleles ‘for’ altruism, to compare with alleles for selfishness. This brings me to my next misunderstanding.
Misunderstanding 4: ‘It is hard to imagine a gene “for” anything so complex as altruistic behaviour towards kin’
The problem results from a misunderstanding about what it means to speak of a gene ‘for’ behaviour. No geneticist has ever imagined that a gene ‘for’ some phenotypic character such as microcephaly, or brown eyes, is responsible, alone and unaided, for the manufacture of the organ that it affects. A microcephalic head is abnormally small, but it is still a head, and a head is much too complex a thing to be made by a single gene. Genes don’t work in isolation, they work in concert. The genome as a whole works with its environment to produce the body as a whole.
Similarly, ‘a gene for behaviour X’ can only refer to a difference between the behaviour of two individuals. Fortunately, it is precisely such differences between individuals that matter for natural selection. When we speak of the natural selection of, for instance, altruism towards younger siblings, we are talking of the differential survival of a gene or genes ‘for’ sibling altruism. But this simply means a gene that tends to make individuals in a normal environment more likely to show sibling altruism than they would under the influence of an allele of that gene. Is that implausible?
It is true that no geneticist has actually bothered to study genes for altruism. Nor has any geneticist studied web-building in spiders. We all believe that web-building in spiders has evolved under the influence of natural selection. This can only have happened if, at each and every step of the evolutionary way, genes for some difference in spider behaviour were favoured over their alleles. This does not, of course, mean there still have to be such genetic differences; natural selection could, by now, have removed the original genetic variance.
Nobody denies the existence of maternal care, and we all accept that it has evolved under the influence of natural selection. Again, we don’t need to do genetic analysis to convince ourselves that this can only have happened if there were a series of genes for various behaviour differences which, together, built up maternal behaviour. Once maternal behaviour, in all its complexity, exists, it takes little imagination to see that only a small genetic change is required to push it over into elder sibling altruism.
Suppose the ‘rule of thumb’ that mediates maternal care in a bird is the following: ‘Feed anything that squawks inside your nest.’ This is plausible, since cuckoos seem to have exploited some such simple rule. Now all that is needed to obtain sibling altruism is a slight quantitative shift, perhaps a small postponement of a fledgling’s departure from the parental nest. If it postpones its departure until after the next brood has hatched, its existing rule of thumb might well cause it automatically to start feeding the squawking gapes that have suddenly appeared in its home nest. Such a slight quantitative postponing of a life-historical event is exactly the kind of thing a gene can be expected to effect. In any case the shift is child’s play compared with those that must have accumulated in the evolution of maternal care, web-building, or any other undisputed complex adaptation. Misunderstanding 4 turns out to be only a new version of one of the oldest objections to Darwinism itself, an objection that Darwin anticipated and decisively disposed of in his section of the Origin on ‘Organs of extreme perfection and complication’.
Altruistic behaviour may be very complex, but it got its complexity, not from a new mutant
gene, but from the pre-existing developmental process that the gene acted upon. There already was complex behaviour before the new gene came along, and that complex behaviour was the result of a long and intricate developmental process involving a large number of genes and environmental factors. The new gene of interest simply gave this existing complex process a crude kick, the end result of which was a crucial change in the complex phenotypic effect. What had been complex maternal care, say, became complex sibling care. The shift from maternal to sibling care was a simple one, even if both maternal and sibling care are very complex in themselves.
Misunderstanding 5: ‘All members of a species share more than 99 per cent of their genes, so why shouldn’t selection favour universal altruism?’
This whole calculus upon which sociobiology is based is grossly misleading. A parent does not share one half of the genes with its offspring; the offspring shares one half of the genes in which the parents differ. If the parents are homozygous for a gene, obviously all offspring will inherit that gene. The issue then becomes: How many shared genes are there within a species such as Homo sapiens? King and Wilson estimate that man and chimpanzee share 99 per cent of their genetic material; they also estimate that the races of man are 50 times closer than are man and chimpanzee. Individuals whom sociobiologists consider unrelated share, in fact, more than 99 per cent of their genes. It would be easy to make a model in which the structure and physiology important in behavior are based on the shared 99 per cent and in which behaviorally unimportant differences, such as hair form, are determined by the 1 per cent. The point is that genetics actually supports the beliefs of the social sciences, not the calculations of the sociobiologists.
This misconception, by another distinguished anthropologist, Sherwood Washburn, arises not from Hamilton’s own mathematical formulation but from oversimplified secondary sources to which Washburn refers. The mathematics, however, are difficult, and it is worth trying to find a simple verbal way of refuting the error.
Science in the Soul Page 18