I am writing a series of posts on the work of George Price. For the most recent one, with links to the others, see here. I was planning next to cover Price’s treatment of group selection, but this raises side issues more conveniently dealt with separately. This post considers what is meant by ‘group selection’. I have tried to establish what various key authors meant by the term (or similar expressions) up to the mid-1970s, when Price’s own work began to be influential.
The concepts of both group selection and kin selection can be traced back to Charles Darwin. I discussed his views at length here. Other biologists of the late 19th century, such as Alfred Russel Wallace, George Romanes, August Weismann and Karl Pearson, were more willing than Darwin himself to assume that natural selection could operate against the direct fitness of individuals, but they seldom considered in any depth how this might work, and so far as I know the term ‘group selection’ was not used. Weismann introduced the curious term ‘Cormal Selection’ (in German ‘Cormal-selektion’): ‘We may distinguish as a fourth grade of selection Cormal Selection, that is, the process of selection which effects [sic] the adaptation of animal or plant stocks or corms, and which depends on the struggle of the colonies among themselves. This differs from personal selection only in that it decides, not the fitness of the individual person, but that of the stock as a whole. It is a matter of indifference whether the stocks concerned are stocks in the actual material sense, or only in the metaphorical sense of sharing the common life of a large family separated by division of labour’ [Weismann, v2, p.378]. The examples Weismann gives (polyps, ants and termites) suggest that he was thinking mainly of species where reproduction is clonal or confined to a specialised reproductive caste.
In the early 20th century evolutionary biology was embroiled in bitter controversies, surveyed in a book by Vernon Kellogg around 1910. I have not read this for the purposes of the present discussion, but on looking through Kellogg’s detailed table of contents I do not see anything directly relevant. Biologists in this period were probably too busy arguing about whether natural selection was important at all to worry much about secondary issues like the levels at which selection operates.
One of the most influential discussions of group selection before the 1930s was written not by a biologist but by the demographer A. M. Carr-Saunders. He collected evidence that families in hunter-gatherer tribes have fewer children than the physiological maximum, and that they regulate their numbers by abortion, infanticide, and abstention from intercourse. He believed that they do this to maintain the size of their group at an optimum in relation to their food supplies. Where many biologists would have been content to mutter ‘for the good of the species’, Carr-Saunders saw the need for a better explanation, and went on: ‘The problem we have to face is how these practices could come to be of the necessary intensity. Now men and groups of men are naturally selected on account of the customs they practise just as they are selected on account of their mental and physical characters. Those groups practising the most advantageous customs will have an advantage in the constant struggle between adjacent groups over those that practise less advantageous customs. Few customs can be more advantageous than those which limit the group to the desirable number, and there is no difficulty in understanding how – once any of these three customs had originated – it would by a process of natural selection come to be so practised that it would produce an approximation to the desirable number’. [Carr-Saunders p.223] This would now be regarded as an example of cultural group selection: those groups with the best customs are most likely to survive and flourish. We may fairly see this as an example of the concept of group selection, but the term itself has not yet appeared. Carr-Saunders’s discussion is cited by several later writers, including V. C. Wynne-Edwards.
The first use of the exact term ‘group selection’ I have found is in R. A. Fisher’s Genetical Theory of Natural Selection (1930). In discussing the origin of ‘the qualities recognized by man as socially valuable’, he says that ‘it has hitherto only been possible to ascribe their evolutionary development to the selection of whole organized groups, comparable to the hives of the social insects. The selection of whole groups is, however, a much slower process than the selection of individuals, and in view of the length of the generation in man the evolution of his higher mental faculties, and especially the self-sacrificing element in his moral nature, would seem to require the action of group selection [my italics] over an immense period’. [p.245] Fisher’s own explanation for ‘socially valuable’ traits avoids group selection. He argues that in primitive societies there is a positive association of fertility and social status, and that individuals showing qualities such as courage, generosity, and honesty would have higher social status, bringing with it higher fertility (more wives, etc) and survival of offspring.
Fisher’s contemporary J. B. S. Haldane also discussed ‘socially valuable but individually disadvantageous characters’. He considered three ways in which such characters could evolve. The first is the special case of parental care. The second is that of social insects. Haldane notes that ‘in a beehive the workers and young queens are samples of the same set of genotypes, so any form of behaviour in the former (however suicidal it may be) which is of advantage to the hive will promote the survival of the latter, and thus tend to spread through the species’ [Haldane p.120]. Finally, he considers the case of ‘small social groups where every individual is a potential parent’. Though he does not use the term ‘group selection’ as such, he develops the first mathematical model of group selection, concluding that it was theoretically possible but required a rather stringent set of conditions to work in the long term.
Fisher’s other great contemporary, Sewall Wright, was more positive about group selection. From 1929 onwards Wright used the term ‘intergroup selection’, and argued that it was important in evolution. I have discussed Wright’s views elsewhere, so will not describe them again, beyond remarking that he did not initially claim that intergroup selection could account for ‘altruistic’ traits. He added this claim only in 1945, saying: ‘it is indeed difficult to see how socially advantageous but individually disadvantageous mutations can be fixed without some form of intergroup selection’ [Wright p.397]. But the evolution of altruism is difficult to reconcile with the process of intergroup selection Wright had previously described. In this process Wright postulates that some local populations (demes) of a species will, by genetic drift and other chance events, produce new and advantageous combinations of genes, giving their members a selective advantage over those of other populations. They will then spread, by expanding their range or by sending out successful migrants. Whether or not this process is plausible in itself, it would not explain the spread of altruism. By definition altruistic individuals are at a selective disadvantage in competition with non-altruists. While it is possible that by genetic drift altruistic traits might reach a high frequency (or even fixation) in some demes, the intergroup selection of altruism seems to require some kind of competition between groups as a whole, and some mechanisms, such as restrictions on interbreeding, or punishment of free-riders, to prevent ‘altruistic’ groups from being contaminated and undermined by non-altruists.
In the 1930s Wright was based at the University of Chicago, which was also the home of the ‘Chicago school’ of ecologists led by W. C. Allee. Allee and his colleagues placed great emphasis on co-operation among animals, for example in his book Animal Aggregations (1931). This work seems to have influenced Wright in believing that altruism was a common phenomenon, and in turn Wright’s endorsement of intergroup selection gave the Chicago ecologists an apparent theoretical basis for their views. The standard work Principles of Animal Ecology (1949) by W. C. Allee, A. E. Emerson, et al, frequently referred to intergroup selection, with reference to Sewall Wright for its justification.
In Britain as well as in the United States many biologists before the 1960s held a vague belief that evolution could work ‘for the good of the species’. There were however some defenders of a more individualistic concept of natural selection, such as E. B. Ford and the ornithologist David Lack. Lack was especially influential in combating the view that the size of animal populations is self-regulated in the interests of the species. The research of Lack and others tended to show that individual animals maximised the number of offspring they could successfully raise [Lack 1954]. By 1960 this was probably the mainstream doctrine. It was however resisted by the British ornithologist V. C. Wynne-Edwards, whose studies culminated in his book Animal Dispersion in Relation to Social Behaviour (1962). (An accessible summary is in his article in Nature.)
It is difficult now to read Wynne-Edwards’s book, not only because it is very long, but because it is exasperating to see his constant invocation of group selection to explain phenomena which usually have obvious explanations by individual, kin, or sexual selection. It is however desirable at least to skim the book, in order to get a sense of why the group selection controversy aroused such passions in the 60s and 70s. As John Maynard Smith plaintively recalled when combating revivals of group-selectionism by Elliott Sober and others, ‘In 1962, when Wynne-Edwards published his book, biology was riddled with “good-of-the-species” thinking… It was quite clear to me, as it must have been clear to George Williams, that no progress would be made toward understanding the evolution of such traits until this kind of thinking was ended… If Sober’s way of describing the world is taken seriously, it will again cease to be obvious, and someone (not me, next time) will have the job to do over again.’ [Maynard Smith, 1987, p.147]
The main thesis of Wynne-Edwards’s book is that a very wide range of animal behaviour, including mating rituals, territory-holding, dominance hierarchies, breeding in colonies, dispersal, and migration, have evolved in order to maintain population size at an optimal level for populations, to avoid exhausting their food supplies. Wynne-Edwards explicitly appeals to group selection to explain these phenomena. (While he sometimes uses Wright’s term ‘intergroup selection’ more often he refers to ‘group-selection’.) For example, he argues that sea birds nest in colonies so that they can assess the size of the population and adjust their breeding to maintain it within the available fishing resources. A necessary component of the theory is that animals exercise ‘prudential restraint’ in the interests of their group as a whole. Of course Wynne-Edwards does not suggest that this is done by conscious calculation, but that groups in which such habits prevail will in the long term survive, while those without such habits will die out. To explain how such traits emerge in the first place, he appeals, predictably, to Sewall Wright’s theory of genetic drift.
Even before Wynne-Edwards’s book was published, W. D. Hamilton was working on his theory of inclusive fitness. (Fisher and Haldane had both anticipated the concept in principle, but had not developed a mathematical theory of it.) In his first short paper in 1963, Hamilton noted that ‘the explanation usually given for such cases [of 'altruistic' behaviour towards individuals other than direct descendants] and for all others where selfish behaviour seems moderated by concern for the interests of a group is that they are evolved by natural selection favouring the most stable and co-operative groups’ [Hamilton p.6] As Hamilton proceeded to show in detail in his papers of 1964, an alternative explanation in terms of inclusive fitness is usually available.
One of the first to see the advantages of Hamilton’s approach was John Maynard Smith. In a short but influential paper in Nature Maynard Smith  coined the term ‘kin selection’, saying ‘it is possible to distinguish two rather different processes, both of which could cause the evolution of characteristics which favour the survival, not of the individual, but of other members of the species. These processes I will call kin selection and group selection, respectively’. He ascribes the concept of kin selection to Haldane and Hamilton, and says ‘by kin selection I mean the evolution of characteristics which favour the survival of close relatives of the affected individual, by processes which do not require any discontinuities in population breeding structure’. ‘Close relatives’ include offspring and siblings, but presumably sometimes more distant relatives.
Maynard Smith says little further about kin selection, and turns to discuss group selection: ‘If groups of relatives stay together, wholly or partially isolated from other members of the species, then the process of group selection can occur. If all members of a group acquire some characteristic which, although individually disadvantageous, increases the fitness of the group, then that group is more likely to split into two, and in this way bring about an increase in the proportion of individuals in the whole population with the characteristic in question. The unit on which selection is operating is the group and not the individual… The distinction between kin selection and group selection as here defined is that for kin selection the division of the population into partially isolated breeding groups is a favourable but not an essential condition, whereas it is an essential condition for group selection, which depends on the spread of a characteristic to all members of a group by genetic drift’. Maynard Smith later discusses the circumstances in which group selection can succeed, using a simplified mathematical model, and concludes, like his mentor Haldane before him, that it requires rather stringent conditions.
Several points about Maynard Smith’s definitions should be noted. First, he applies both kin and group selection only to ‘characteristics which favour the survival, not of the individual, but of other members of the species’. Selection which goes in the same direction at both individual and group level is therefore ignored, presumably not because it cannot happen but because it presents no interesting problem. Second, Maynard Smith’s definition of kin selection does not require that the behaviour of ‘altruists’ is directed preferentially towards relatives, but only that its effect is to favour them (for example because they are geographically concentrated). This point was sometimes misunderstood by later writers. Third, the definition of kin selection explicitly includes parental care. Fourth, the definition of group selection requires separation of the population into partially isolated groups. Finally, Maynard Smith confines group selection to cases where some groups consist entirely of altruists, as a result of genetic drift.
These last two points imply a rather narrow definition of group selection. Later writers have devised models, which they describe as models of group selection, in which groups are not geographically isolated, or which contain a mixture of altruists and non-altruists, but where altruism still prevails. Maynard Smith himself criticised this wider usage of the term group selection, mainly because he believed that it blurred the distinction between group and kin selection, as in such models the success of altruism often depended on the geographical proximity of relatives. But this criticism was not always valid, as there are at least some models in which altruism can prevail without help to relatives.
The other critics of Wynne-Edwards’s theory included C. S. Elton, David Lack and George C. Williams. Elton, Britain’s leading animal ecologist, sceptically reviewed Wynne-Edwards’s book, pointing out that animal populations often fluctuated widely, with little sign of ‘self-regulation’ [Elton 1963]. Lack’s contribution [Lack 1966] was primarily to survey the empirical evidence for alternatives to group selection in explaining animal behaviour. Williams covered both empirical and theoretical aspects, with an entire chapter of his book devoted to group selection (a term which he attributes to Wynne-Edwards [Williams p.96]) and several others dealing with specific aspects of the problem. Like Maynard Smith, Williams is concerned only with cases where selection at the level of the group seems to act against the interest of individuals, and he specifies that ‘a group in this discussion should be understood to mean something other than a family and to be composed of individuals that need not be closely related’ [p.93]. In general he is even more sceptical than Maynard Smith about the importance of group selection, stressing that it should only be invoked ‘when the simpler explanation is clearly inadequate’ [p.124]. He does however appear to accept that over the very long term (geological time) group selection at the level of species as a whole could be important in the pattern of evolution. [p.97-101]
The work of George C. Williams brings us almost to the time at which George Price entered the debate on group selection. Price’s work however made little impact until the mid 1970s. In particular, his papers on ‘Price’s Equation’, and its application to group selection, are not mentioned in E. O. Wilson’s book Sociobiology: the New Synthesis (1975). It will therefore be worth looking briefly at the treatment of group selection in this. At the outset of his discussion Wilson adopts a very broad definition of group selection: ‘selection can be said to operate at group level, and deserves to be called group selection, when it affects two or more members of a lineage group as a unit’. However, within this broad definition he distinguishes between kin selection and ‘interdemic’ selection: ‘If selection operates on any of the groups [of relatives] as a unit, or operates on an individual in any way that affects the frequency of genes shared by common descent in relatives, the process is referred to as kin selection. At a higher level, an entire breeding population may be the unit, so that populations (that is, demes), possessing different genotypes are extinguished differentially, or disseminate different numbers of colonists, in which case we speak of interdemic (or interpopulation) selection’ [p.106].
Curiously, in the Glossary to his book Wilson defines kin selection as ‘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 gene by common descent…’ [p.587]. The exclusion of offspring from kin selection does not seem consistent either with Wilson’s own earlier definitions, with Maynard Smith’s original definition of kin selection, or with Hamilton’s concept of inclusive fitness. Wilson’s rationale for the exclusion may have been that offspring contribute to an individual’s own reproductive fitness, so that help given to offspring is covered by conventional Darwinian natural selection without any need for the concept of kin selection. But this is an oversimplification if there is any choice in the allocation of an individual’s resources between producing new offspring, helping existing offspring, and helping other relatives. In this situation the principles of inclusive fitness have to be applied to explain why, for example, it is usually better to help offspring than nephews.
To draw a few conclusions from this brief survey:
1. The term ‘group selection’ itself was seldom used before the 1960s, though Wright’s term ‘intergroup selection’ was used by various authors.
2. There was very little serious analysis of the concept of group selection before Wynne-Edwards’s book and the subsequent controversy. The only quantitative approach, so far as I know, was that of Haldane. The remarks of Fisher and Wright on the subject were vague and qualitative. Sewall Wright’s authority, however, was such that his acceptance of group selection was influential on other biologists, especially in America.
3. The introduction of the concept of inclusive fitness by Hamilton (and Maynard Smith’s handy terminology of ‘kin selection’) brought about a useful clarification. There was little prospect for a useful discussion of group selection so long as biologists failed to distinguish between cases such as the social insects, where close genetic relatedness is important, from cases (real or hypothetical) where group selection does not depend at all on relatedness.
4. Even after the debates of the 1960s, there was no uniformity of usage in the definition of group selection – E. O. Wilson, for example, had a different usage from Maynard Smith. (I would add that there was also disagreement over the definition of altruism, but that is a subject for another post.) The continuing controversy in the 70s and beyond has been aggravated by the confusion of semantic and substantive issues.
Added on 16 January: In comments Peter Mazsa has linked to a Google Books text search for the phrases ‘group selection’ and ‘intergroup selection’. This shows some uses of these terms going back to the 1890s. As I would have expected, there is a great surge in the use of ‘group selection’ after 1960, but I was surprised to see that between 1930 and 1960 there are more results for ‘group’ than ‘intergroup’ selection. I have looked at some of the detailed search results and find there is a snag in interpreting these data, as the phrase ‘group selection’ had several technical uses in contexts quite unconnected with its use in evolutionary biology, for example in forestry, telephony, insurance and psychotherapy! These uses probably account for the majority of results before 1960. But there are certainly also some relevant biological uses from this period. The earliest I have so far identified is in an essay of 1895 by the sociologist and political philosopher Bernard Bosanquet. His comments are quite interesting and I may do a separate note on them.
Pearson does not use the exact phrase ‘group selection’, but does use the terms ‘intra-group selection’ and ‘extra-group selection’. Intra-group selection is selection within a group resulting from competition between its members. Extra-group selection (meaning literally outside-group selection) could mean selection between individual members of different groups, but it is clear from the context that Pearson intended it to mean primarily selection between groups as a whole. Pearson regarded himself as a socialist as well as a good Darwinian, and was keen to rebut claims that socialism was incompatible with natural selection. Pearson argued that as human society becomes more advanced, competition and selection within groups becomes less important, as it gives way to co-operation and collective action, whereas competition and selection between groups (tribes, nations or races) becomes even stronger.
These early writers on group selection seldom gave much attention to the problem raised, but not solved, by Charles Darwin in the Descent of Man: if the qualities promoting group success, such as co-operation and self-sacrifice, conflict with individual success within the group, how is the conflict resolved? Bernard Bosanquet’s essay does however at least address the problem. His answer is essentially that there is no conflict. As society evolves, it creates a new selective environment for individuals, and this favours co-operation: ‘the struggle for existence has, in short, become a struggle for a place in the community; and these places are reserved for those individuals which in the highest degree possess the co-operative qualities demanded by circumstances’ (p.294). One may wonder if this assertion would stand up to close empirical testing, but Bosanquet deserves credit for recognising a problem generally ignored.
W. C. Allee: Animal Aggregations: a study in general sociology, 1931
W. C. Allee, A. E. Emerson, et al.: Principles of Animal Ecology, 1949
A. M Carr-Saunders: The Population Problem, 1925
C. S. Elton: Review of Wynne-Edwards, Nature, 1963, 197, p.634
R. A. Fisher: Genetical Theory of Natural Selection: a complete variorum edition, ed. Henry Bennett, 1999.
J. B. S. Haldane: The Causes of Evolution, 1932, Princeton UP edition 1990
W. D. Hamilton: Narrow Roads of Gene Land, vol. 1, 1996
Vernon Kellogg: Darwinism Today, 1907
David Lack: The Natural Regulation of Animal Numbers, 1954
David Lack: Population Studies of Birds, 1966
John Maynard Smith: ‘Group Selection and Kin Selection’, Nature, 1964, 201, p.1145-7
John Maynard Smith: ‘Reply to Sober’ in The Latest on the Best: Essays on Evolution and Optimality, ed. John Dupre, 1987
August Weismann: Lectures on the Evolution Theory, English edn., 1904
George C. Williams: Adaptation and Natural Selection, 1966
E. O. Wilson: Sociobiology: the New Synthesis, 1975
Sewall Wright: Evolution: Selected Papers, edited and with Introductory Materials by William B. Provine, 1986
V. C. Wynne-Edwards: Animal Dispersion in Relation to Social Behaviour, 1962
V. C. Wynne-Edwards: ‘Intergroup selection in the evolution of social systems’, Nature, 1963, 200, 623-6