What Darwin Said: Part 7 – Levels of Selection

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This is the seventh and last in a series of posts about Charles Darwin’s view of evolution. Previous posts were:

1: The Pattern of Evolution.
2: Mechanisms of Evolution.
3: Heredity.
4: Speciation
5. Gradualism (A) , which dealt with Darwin’s views on gradualism in the rate of evolutionary change.
6. Gradualism (B), about the size of the mutations adopted by natural selection.

This final post deals with Darwin’s views on the levels of selection in evolution. Does selection occur mainly between genes, individuals, families, groups, species, or what? In the modern debate on levels of selection, Darwin has been quoted in support by both sides: those who accept, and those who reject, a major role for selection above the level of the individual organism.

Unless otherwise stated, all page references are to Charles Darwin: The Origin of Species: a Variorum Text, edited by Morse Peckham, 1959, reprinted 2006.

This post will be (relatively) brief, because there is already an excellent detailed study [Ruse] which I have little to add to.

Darwin’s position on levels of selection can be summarised in four points:

1. His formulation of the process of natural selection is expressed almost entirely in terms of selection among individuals, based on what he calls ‘individual differences’. In this respect he differs from Wallace, who referred mainly to selection between ‘varieties’. It has recently been argued that Wallace (in 1858) did not quite ‘get’ the idea of natural selection after all. Be that as it may, Wallace was always more welcoming than Darwin to what we would now call group selection.

2. Darwin gave no autonomous role to selection between species or varieties. In so far as he did mention selection at these levels, it was as a by-product of selection at lower levels. For example, if a newly introduced species displaces an indigenous one, it is because the individual organisms of the first species are competitively superior to those of the second.

3. Darwin recognised the possibility that selection might operate on individuals indirectly, via the individual’s relatives, as in the case of neuter insects. Thus he had the germ of the modern ideas of kin selection and inclusive fitness, but these were not fully developed until much later.

4. At a level between the family and the species, Darwin recognised a role for selection between social communities, notably among social insects and human ‘tribes’. Most of the recent debate about Darwin’s views on levels of selection has concerned the interpretation of this ‘community selection’.

Darwin’s most explicit statement on the issue in the Origin says in the first edition (with italics added):

Natural selection will modify the structure of the young in relation to the parent, and of the parent in relation to the young. In social animals it will adapt the structure of each individual for the benefit of the community; if each in consequence profits by the selected change [172]

In the fifth edition the word each is revised to this and in the sixth to the community. It has been suggested [Richards p.217] that these changes involve an important shift towards group selectionism. In the first edition, traits benefiting the community are only selected if they are also beneficial to the individual, but in the fifth and sixth editions such a trait can be selected if even if it is harmful to the individual. I agree that this is an important revision, but I think it is only stating as a general principle something that Darwin had already accepted in individual cases. He believed that the sterility of neuter insects had been selected for the good of the community [417]. Likewise, the sting of bees is useful to the community, and is selected for that reason, even though it kills the individual bee when it is used [374]. Since dying, or becoming sterile, are clearly against the interests of the individual, these examples were inconsistent with Darwin’s original formulation, and his revisions may just have been a belated recognition of this.

If a trait is beneficial to the community, but harmful to the individual who possesses the trait (like the bee’s sting), the question arises how such a trait can increase in frequency. In the case of the sterile classes of social insects Darwin saw fairly clearly that the solution was in the relatedness of the members of the colony:

This difficulty, though appearing insuperable, is lessened or, as I believe, disappears, when it is remembered that selection may be applied to the family, as well as to the individual, and may thus gain the desired end… Thus I believe it has been with social insects: a slight modification of structure, or instinct, correlated with the sterile condition of certain members of the community, has been advantageous to the community: consequently the fertile males and females of the same community flourished, and transmitted to their fertile offspring a tendency to produce sterile members having the same modification [416-17].

The same mechanism does not apply where individuals are not genetically related. In the fifth edition Darwin discussed the problem in the context of the sterility of hybrids:

With sterile insects we have reason to believe that modifications in their structure and fertility have been slowly accumulated by natural selection, from an advantage having been thus indirectly given to the community to which they belonged over other communities of the same species; but an individual animal not belonging to a social community, if rendered slightly sterile when crossed with some other variety, would not thus itself gain any advantage or indirectly give any advantage to the other individuals of the same variety, thus leading to their preservation [445]

Darwin concluded (contrary to the position of Wallace) that the sterility of hybrids, and the inter-sterility of different species, had not evolved directly by natural selection but as a by-product of other changes. Unfortunately in the sixth edition the quoted passage was omitted, as Darwin believed he had more convincing new evidence that the sterility had not been selected.

In the Descent of Man, Darwin returned to the issue in the context of the evolution of human morality. He believed that tribes containing ‘a greater number of courageous, sympathetic, and faithful members’ [Descent of Man, 1871, p.162] would succeed in competition against other tribes, but he saw a problem in explaining how such virtues could evolve within a tribe: ‘But it may be asked, how within the limits of the same tribe did a large number of members first become endowed with these social and moral qualities, and how was the standard of excellence raised?’ [163] He thought it was very unlikely that these qualities could be directly favoured by natural selection within a tribe. As a ‘probable’ solution, he suggested two important factors. One was what we now call ‘reciprocal altruism’, i.e. that a benefit might be provided in the expectation of a return benefit [163]. To complicate matters, Darwin believed that habitual behaviour, once acquired, could be transmitted by ‘Lamarckian’ inheritance [163-4]. The second, and more important, factor was ‘the praise and blame of our fellow-men’ [164]: ‘it is hardly possible to exaggerate the importance during rude times of the love of praise and the dread of blame’ [165]. Darwin does not explain how praise and blame are converted into individual fitness, but modern theorists have devised game theoretical models to handle these issues, which tend to confirm the importance of reputation. An individual who gains a reputation as a cheat or shirker will be excluded from the benefits of social life, with adverse effects on fitness.

Finally, Darwin returns to the point that tribes with many individuals possessing traits of courage, etc, ‘would be victorious over most other tribes; and this would be natural selection’ [166]. This passage is the main basis for the claim that Darwin became a ‘group selectionist’. In a sense this is true, since it does give selection between groups (tribes) a role in promoting the spread of a trait. However, I do not think Darwin intends it as part of the solution to the question ‘how within the limits of the same tribe did a large number of members first become endowed with these social and moral qualities’. If he did, the solution would clearly be invalid. The process of group selection envisaged by Darwin presupposes that some tribes already have ‘many individuals’ possessing the qualities in question. At best group selection has a role in reinforcing and extending the prevalence of altruistic traits which have first emerged within the tribes for other reasons.

The crucial problem for group selectionists has always been to explain how altruistic traits can become common within a group despite harming individual fitness. Darwin sidesteps the problem in this form, since his two suggested mechanisms (reciprocal altruism and ‘praise and blame’) in fact raise individual fitness, perhaps sufficiently to offset the loss of fitness. The problem of altruism still remains for those theories in which altruists suffer a net loss of individual fitness. If ‘genes for altruism’ are randomly distributed, and the benefits of altruism are simply proportional to the number of altruists in the group, then altruism will always be eliminated (apart from recurrent mutations) [Maynard Smith p.166]. A solution is however possible if either (a) genes for altruism are concentrated in some groups above chance levels, for example because close relatives tend to live near each other; or (b) the benefits of altruism are not simply proportional to the number of altruists. If chance concentrations of altruists gain disproportionate benefits, altruism can be selected despite its fitness detriment to those altruists who fall outside such concentrations. ‘Synergistic’ effects of this kind are quite plausible [Maynard Smith p.167], yet this solution to the problem has been strangely neglected.

Group selection of some kind is therefore possible, and it is an empirical matter to determine its prevalence and the mechanisms responsible in any particular case. Darwin did not solve the problem, but at least it may be said that he recognised it more clearly than any evolutionist before R. A. Fisher, and that he sketched out most of the possible solutions to the problem that have been explored more fully by his successors.

This post brings to an end my series of posts on ‘What Darwin Said’, which I regard as my contribution to ‘Darwin Year’. I have not aimed to cover every aspect of Darwin’s work, even in evolutionary theory – notably, I have not discussed sexual selection. I hope however that I have clarified Darwin’s views on most of the issues that are still under serious debate. I have also tried to evaluate how far Darwin’s views have stood the test of time. Overall, I think the answer is ‘remarkably well’, considering the extent of ignorance and false beliefs in Darwin’s time on many key issues such as the nature of inheritance. But Darwin was not infallible, even with the evidence available to him, and it would be short-sighted to defend evolutionism in general by pretending (in the manner of diehard Marxists) that the Master was always right.

John Maynard Smith, Evolutionary Genetics, 1989.
Robert J. Richards, Darwin and the Emergence of Evolutionary Theories of Mind and Behavior, 1987.
Michael Ruse: ‘Charles Darwin and Group Selection’, Annals of Science, 37, 1980, 615-30, repr. in The Darwinian Paradigm, 1989.


  1. Nice post, I’ve enjoyed the series! 
    By chance (I’m guessing) this comes while David Sloan Wilson, the newest addition to ScienceBlogs.com, is talking about group selection. So far he’s giving a sort of history of group selectionism and its various incarnations (I don’t know where he’s headed, but we’ll see I guess). You may find his posts interesting: 
    #1: http://scienceblogs.com/evolution/2009/10/truth_and_reconciliation_for_g.php 
    There’s 5 so far as I’m writing this comment

  2. I really enjoyed your Darwin series, David. Thanks.

  3. bravo!

  4. Thanks for the link to D. S. Wilson’s stuff. Maybe it will get better in later episodes!

  5. In the case of the sterile classes of social insects Darwin saw fairly clearly that the solution was in the relatedness of the members of the colony: 
    This raises all kinds of conceptual trouble. 
    Technically it is true that some degree of relatedness is necessary for the maintenance of eusociality. Imagine you take a couple colonies of social insects, and then, at every generation, you randomly reassign sterile workers among colonies, all other things remaining equal. This has the effect that workers in a colony are unrelated to their queens, or to each other. What would happen then? Well, eusociality would eventually fade away. Queens / colonies that beget good workers would not have any reproductive advanatge over those that beget lazy, feeble, or even (Heaven forbid) fertile workers. As a result, their genes would not be favoured, natural selection for good (cooperative) workers would not occur, and eusociality would decay in mutational meltdown. 
    This is why the two Wilsons’ insistence that group selection is a valid, autonomous explanation for the maintenance of eusociality (let alone its emergence) is difficult to understand. The thought experiment above isolates the effects of “pure” group selection – and demonstrates their inability to maintain eusociality. “Group selection” only works in association with (one could say “as a crutch to”) kin selection. 
    And yet… 
    Notice that in eusocial colonies, individuals are completely dependent on each other. If they start reproducing selfishly, they can be successful while the colony survives, but cannot escape from it. When the colony finally collapses, they perish with it. The situation is exactly equivalent to that of cells within a multicellular body – they can start reproducing selfishly, and be successful within the body (that’t what we call “cancer”), but once the body dies, they die with it. It’s almost (almost) impossible for cheaters to survive and thrive in the long term. 
    Yet we have no qualms in stating that the delicate organisation of the human body is maintained by individual-level selection (that is, selection at the level of groups of cells), but somehow when it comes to social insects we insist that kin selection is important and that group selection (that is, selection at the level of the colony) cannot suffice as an explanation. 
    It’s not easy to see the objective difference between the two cases.

  6. Of course group selection exists. It would seem to be the most important mechanism shaping human evolution. There are hundreds of known examples of one human population replacing another. This is group selection in its purest form. Granted, that the fitness advantage involved was more likely to be cultural than genetic–that doesn’t alter the fact that the population replacement happened and had genetic consequences. 
    In animals without a culture, the results are likely to be less dramatic, but they certainly happen. When one variety of a species begins to expand its range as a result of changing conditions, it will change the gene pool of the whole species of which it is a part. I really don’t see any point in denying this. Is it just squeamishness about the social-political implications?

  7. Toto: as usual, a lot of the argument is about semantics. If selection occurs between single-queen colonies, is it useful to describe that as ‘group selection’, rather than individual selection between the queens (and their mates), with the sterile workers regarded merely as their ‘bodies’? 
    The debate only really gets interesting (IMHO) with respect to the origins and maintenance of eusociality itself. I am not sure that the analogy with cancer goes very far. Cancer cells are not capable of leaving one body and forming a new body of their own. In contrast, if a worker lays fertile eggs (which can happen in many species), the individuals hatched from those eggs could in principle found new colonies (or, if male, mate with queens). This is usually suppressed (I think) either by the queens or by other workers. The question is whether there is a non-trivial role for group selection in explaining this. I’m not sure that there is, but it is probably an open question. Of course, competition between colonies is an important part of the selection pressure on queens, but surely no-one has ever doubted that.

  8. DavidB, 
    I totally agree, I simply want to add that there are cases of cancers that can survive the death of their ‘hosts’, for example in the Tazmanian Devil, and I’m pretty dure that there’s something similar in dogs. And, of course, HeLa cells (a ca. 30 year old cancer cell line) grow like weeds and often ‘infect’ (contaminate) other cell cultures, but they’re not ‘natural’ so I guess they don’t count.

  9. David, what Toto says applies not only to tumors, though, but also to microbes – which of course have lineages that go on indefinitely. Cooperation between clonal cells or virions with almost perfect sequence identity has been put forward as a group-selected trait. Like Toto, I blush to hear such things because it just seems totally obvious that this is kin selection.  
    At any rate, I see Toto’s cancer example as valid, anyway. Most tumors may not live very long, but our lineages won’t last forever either. I don’t see a qualitative difference.

  10. A case of cancer cells ‘escaping’ in humans: http://www.webmdhealth.com/nl/nlv.aspx?id=gbfenrIjkyM=&s=10554 
    Leukemia cells from a mother found in her baby. Admittedly though, those leukemia cells aren’t going to go any further…