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June 01, 2005

Group Selection (oh no, not again!)

In a recent post on Altruistic Punishment I remarked that ‘group selection should be regarded as an explanatory last resort’.

I didn’t intend this to be a controversial proposition, but as some comments challenged it, I will give some reasons for regarding group selection as a last resort.

I will assume that the traits favoured by group selection (whatever that means) are not independently favoured by selection on individuals. The whole point of the group selection debate is about how to explain traits that appear contrary to individual selection.

[Added on June 2: Of course, I am not denying that in some circumstances a trait could be favoured by selection at both individual and group level, but this is not very interesting, and it is not what the group selection controversy is about. As George C. Williams put it: ‘Many biologists have implied, and a moderate number have explicitly maintained, that groups of interacting individuals may be adaptively organized in such a way that individual interests are compromised by a functional subordination to group interests. It is universally conceded by those who have seriously concerned themselves with this problem that such group-related adaptations must be attributed to the natural selection of alternative groups of individuals and that the natural selection of alternative alleles within populations will be opposed to this development… 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’ (Adaptation and Natural Selection, 1966, p.92) If people insist on using the term ‘group selection’ for cases where individual selection within the group is favourable, or at least neutral, towards the trait in question, then I think they should at least use some additional qualifying term. I suggest that it should be called Trivial Group Selection, by analogy with mathematical usage, where problems often have ‘trivial’ solutions for some values of the variables. For example, the equation in Fermat’s Last Theorem has solutions for x = y = z = 0, but Andrew Wiles would have won no prizes for pointing this out.]

Beginning with some points of methodology:

1. By their fruits ye shall know them (Matthew 7: 20). In assessing any scientific theory we should ask whether it has proved fruitful. In Imre Lakatos’s terms, is it a progressive research programme? Is it generating testable empirical hypotheses and predictions, and if so, are they turning out successfully? Modern group selection theories have been under discussion for over 30 years now, but apart from M J Wade’s experiments on flour beetles (which present the most favourable circumstances for group selection) they seem to have generated little in the way of empirical data. If we look back further in time, group selectionism of the old kind was not only unfruitful but an obstacle to the progress of evolutionary theory. As John Maynard Smith said some years ago in a critique of Elliott Sober, until the 1960s ‘biology was riddled with “good-of-the species” thinking. Again and again, one met in the literature explanations of some trait… in terms of the benefit that the trait conferred on the species, or even on the ecosystem as a whole. It was 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’ (ref.1).

2. Theories are not to be multiplied without necessity. Since we clearly do need selection at individual level, it would be more parsimonious if we can also use it to explain the phenomena (such as ‘altruistic punishment’) for which group-selectionist hypotheses are being offered. We should look carefully for individual-selection solutions, such as inclusive fitness or game theory, before resorting to group selection.

3. Models of group selection are more complex than those of ordinary selection, because they have to incorporate at least two levels of selection and the interactions between them. They also tend to involve unfamiliar concepts and terminology. The objection to this is not just the effort involved in learning and applying any complex new theory, but the difficulty of interpreting the results. For an example see here.

4. Much of the argument about levels of selection has been about words rather than facts. The term ‘group selection’ by itself can cover many quite different phenomena. In considering any proposed application of group selection to some trait, we need to ask:

- is the trait cultural or genetic?
- is it a trait of a group or of individuals?
- is differential reproduction occurring at the level of the group (e.g. by group extinction or multiplication) or at the level of individuals?
- if a trait of individuals varies in frequency between different groups, how does the variance in frequency arise, and how is it maintained in the face of migration and interbreeding?
- is the trait selected by virtue of its own effects on the fitness of groups or individuals, or as a by-product of other properties?

To illustrate the last point, it is obvious that some human cultural traits have spread because they happen to be linked to successful political entities, the success of which has little or nothing to do with the traits in question. For example, the English language is widely spoken throughout the world, while Italian is not, but no-one will suppose that this has much to do with the intrinsic merits of English compared to Italian. Some authors distinguish between ‘selection’ and ‘sorting’ of traits, where ‘sorting’ does not imply any intrinsic fitness advantage of the trait concerned. In these terms English has spread through sorting but not selection. There is no doubt that ‘sorting’ in this sense does occur, but it is not very interesting, and we don’t need any elaborate theory to explain it. It is not what the group selection controversy is about.

Depending on the answers give to the questions above, many different versions of group selection can be proposed, some of which are more plausible than others. Watch out for the old ‘bait-and-switch tactic’. Also watch out for the use of the label ‘group selection’ for phenomena that would not be generally recognised as group selection at all. Notably, if a trait is selected by virtue of its fitness effects within local concentrations of genetically related individuals, many would call this kin selection rather than group selection.

Moving on to objections of substance, it is difficult to generalise because different objections apply to different versions of group selection:

5. In the older theories of group selection, differential reproduction was usually defined in terms of the extinction or multiplication of groups as a whole. The main difficulty with this is that a group would normally have a ‘generation time’ much longer than that of individual organisms. If the groups contain genetically diverse individuals, the traits favoured by individual selection would therefore (other things being equal) increase in frequency more quickly than those favoured by group selection. In order for group selection to prevail, the groups have to be very pure to begin with, mutation and migration rates have to be low, and/or the group selection effect per ‘generation’ has to be strong compared with individual selection. If we are dealing with human evolution, there is also the problem that there just may not have been enough time for extinction or multiplication of groups to have had much effect. Cultural evolution in particular often occurs within a group ‘lifetime’, so it is very difficult to see how group selection of this kind could explain it.

6. In the newer theories of group selection (from about 1975 onwards), the selective process usually depends on the differential reproduction of individuals rather than groups. In these theories groups as such do not ‘die’ or ‘give birth’, but individuals vary in fitness according to the frequency of certain traits within groups. The ‘group selection’ effect therefore depends on covariance between fitness and frequency of the trait within groups. Price’s Equation, which I discussed here, provides a framework within this can be analysed. The difficulty for group selectionists is to explain how sufficient covariance is maintained despite migration and mixing of groups. Generally speaking, models of this kind only work if groups are small and fairly isolated. It then becomes difficult to distinguish group selection from kin selection, since the members of the group will often be related to each other.

7. Group selection is complicated. Cultural evolution is also complicated. When people try to combine the two in ‘cultural evolution by group selection’ I despair. I commented at length on the difficulties here, over 2 years ago. I wouldn’t still agree with all the details, but I don’t see any reason to change the general thrust. There are just too many differences between genetic and cultural evolution for the analogy to be useful. And one of the few actual examples of cultural group selection that is ever used by the Groupies - the Nuer Conquest - turns out on investigation to be much weaker than they claim.

8. As far as I recall, I have never seen a model of group selection that deals with the selection of more than one trait at a time. This is a problem even for selection on individuals. In a classic 1957 paper on the ‘cost of natural selection’ J B S Haldane estimated the number of ‘selective deaths’ (or failures to reproduce) that would be necessary in order for a rare advantageous gene to spread to fixation, and concluded that with plausible levels of advantage it would take about 300 generations per locus. If many loci were under selection simultaneously the process would take much longer. Later geneticists argued that Haldane’s assumptions were oversimplified, and that with more complex (but biologically reasonable) assumptions about the mode of selection it would be possible for a larger number of genes to be fixed more quickly (see e.g. refs. 2 and 3). But the problem is more severe for group selection because most models require the effect of a trait on group fitness to be large, in order to overcome countervailing individual selection. If a group has more than a few favourable traits under selection simultaneously, the combined effect on fitness could be unfeasibly large. There is also the difference that in individual selection a species will typically contain millions of individuals, much more than the number of loci under selection (which cannot be more than the number in the species genome). In contrast, with group selection the number of traits (cultural or genetic) under selection may be of the same order of magnitude as the number of competing groups (probably no more than a few hundred in the same geographical area). This poses additional problems for the ‘cost of selection’. I don’t know if the problems are insuperable, but my guess is that group selection can only effectively promote a few traits at a time.

It is still conceivable that group selection might account for one or a few particularly important human traits, such as language, social conformism, or collective punishment, which would then have a multitude of secondary effects by creating new conditions for evolution by individual and kin selection. But I hope we can do without it, and the onus of proof is on those who say we cannot.

Ref. 1: John Maynard Smith, ‘Reply to Sober’, in The Latest on the Best: Essays on optimality and evolution, ed. John Dupré, 1897.
Ref. 2: John Maynard Smith, ‘ “Haldane’s Dilemma” and the rate of evolution’, Nature, 1968, 219, 1114-1116.
Ref. 3: P. O’Donald, ‘ “Haldane’s Dilemma” and the rate of natural selection’, Nature, 1969, 221, 815-7.

Posted by David B at 06:41 AM