Saturday, February 23, 2008

Group Selection and the Wrinkly Spreader   posted by DavidB @ 2/23/2008 06:28:00 AM

A recent article by D. S. and E. O. Wilson [1] has been acclaimed by some as reviving the fortunes of group selection. It must for a time have been available on the web (since I downloaded a pdf of the published version a month or so ago), but the closest thing I can find at present is this slightly different version submitted to (and presumably rejected by) Science in 2006. [Added: I should perhaps have mentioned that the two Wilsons are not related. No kin selection here!]

As gnxp's resident critic of group selection I feel an obligation to say something about the article, but I find the task dispiriting. Much of the Wilsons' article is a re-working of issues which have been debated many times before. (See e.g. my discussion here.) The debate has been largely about the most useful way of describing and classifying the phenomena, rather than about the biological facts. Hostility to group selectionism is provoked in part by the tendency of its advocates to claim for group selection a range of phenomena that other biologists regard as more usefully described in terms of inclusive fitness (kin selection). This hostility will not be allayed by such prominent assertions as:

During evolution by natural selection, a heritable trait that increases the fitness of others in the group (or the group as a whole) at the expense of the individual possessing the trait will decline in frequency within the group.

If the 'group' contains local concentrations of relatives (as it very often will), or if the trait preferentially affects relatives, this assertion is simply not correct. Did the Wilsons not notice this, or were they deliberately loading the dice against interpretations in terms of kin selection? Another potential confusion of the issues comes later in the article, where the Wilsons discuss insect eusociality. They argue strongly that between-colony selection is important in the evolution of eusocial insects, for example in traits such as nest construction. But whoever doubted it? Once eusociality (specialisation of reproduction) has been established, of course genetic variation and selection will often be between different colonies. The difficult question is how eusociality itself becomes established. The important insights into this have come from inclusive fitness theory, not group selectionism. (See for example chapter 11 of [2].)

Rather than spend more time on arid and abstract theoretical issues, I think it will be more rewarding to focus on a single empirical case, which the Wilsons themselves offer as a good example of the benefits of a multi-level approach. It can therefore serve as a test case of the benefits of that approach. The example I have chosen is the Wrinkly Spreader...

As the Wilsons describe this case,

the "wrinkly spreader" (WS) strain of Pseudomonas fluorescens evolves in response to anoxic conditions in unmixed liquid medium, by producing a cellulosic polymer that forms a mat on the surface. The polymer is expensive to produce, which means that non-producing 'cheaters' have the highest relative fitness within the group. As they spread, the mat deteriorates and eventually sinks to the bottom. WS is maintained in the total population by between-group selection, despite its selective disadvantage within groups, exactly as envisioned by multi-level selection theory.

I have followed up the Wilsons' reference for this case, and then some other citations. [Refs. 3, 4, and 5]

The facts of the WS case (stripped of theoretical baggage) seem to be as follows.

Pseudomonas fluorescens is a rod-shaped flagellated aerobic bacterium. It is found widely in the soil and in fresh water. In nature it is normally found as a single free-moving cell. In laboratory cultures, on the other hand, it often develops mutant strains which stick together rather than living singly. One of these is the Wrinkly Spreader strain, so-called because on slides of nutrient jelly it spreads out in sheets with a distinctive wrinkly appearance. In open containers (e.g. test tubes) of nutrient fluid the WS bacteria form a mat on the surface. Within about 10 days the mat becomes too heavy and sinks to the bottom. If the supply of nutrient is adequate, the process may be repeated, with new WS mats forming and eventually sinking.

Rainey and colleagues have studied the genetics of the WS strain.[3, 4 and 5] They have found that WS bacteria produce an excess of a cellulosic polymer which causes them to stick to each other and to surfaces. A side-effect of this is that they form a scum at the liquid-air interface (I presume this is a surface-tension effect, but the precise mechanism does not matter.) The production of the polymer uses scarce resources, so WS bacteria reproduce more slowly than non-WS bacteria in the same circumstances. However, this is offset by the advantage of being able to colonise the surface layer, with its better access to oxygen.

The description so far assumes that the mats on the surface contain only WS bacteria, usually derived from a single mutant individual. WS bacteria within the mat may however mutate in various ways which stop them overproducing the polymer, so that they revert to the ancestral phenotype. These mutants reproduce more quickly than the WS strain. They therefore tend to spread within the mats. But this weakens the structural integrity of the mats, which causes them to break up and sink more rapidly than the pure WS mats.

So what has this to do with group selection? What are the 'groups', and where is the 'selection'?

I think it will help to divide the cycle into two stages: before and after the emergence of non-WS mutants within the mats. At the beginning of the process, there are only single bacteria. Some of these mutate to the WS form, and literally stick together. Within the broth culture as a whole, WS mutants have lower fitness than the ancestral form, but the mutation gives them characteristics which enable them to predominate in a particular part of the ecosystem, i.e. the surface layer. Rainey et al. describe this as a form of 'cooperation', in which 'cooperation is costly to individuals, but beneficial to the group'. They note that the WS individuals are closely related (since they are descended from the same mutant individual) and describe the trait as spreading by 'kin selection'. This seems to me an unnecessary interpretation. The WS individuals in the surface layer are not sacrificing any fitness for the benefit of other individuals: they are simply using resources in a way that enables them to occupy this part of the environment. In a heterogeneous environment it can be misleading to average fitness over the entire range of sub-environments. For analogy, suppose a species of sheep ranges over a variety of altitudes. At higher altitudes the climate is colder, and the sheep need thicker fleece to live there in the winter. Sheep with mutations causing them to grow thicker fleece may have lower fitness than the average sheep, because it is costly to grow thick fleece, but at high altitudes the thick-fleeced variant may predominate because it is better adapted to that particular environment. Similarly, the WS strain is better-adapted to the surface layer. It is merely a coincidence that the adaptation involves the formation of 'groups'. We could imagine that instead of producing a polymer, and sticking together, the mutants produced little bubbles of gas which enabled them to float at the surface. In this case, no-one would dream of describing the process as either kin or group selection.

There is a more plausible case for appealing to group selection in the later stage of the process, when non-WS individuals have emerged within the WS mats. These individuals obtain the advantage of living in the surface layer without paying the cost. It is therefore reasonable to describe them as 'cheaters' or 'defectors'. They reproduce more rapidly, for a while, but in the longer term destroy the mats, to the detriment of all. According to the Wilsons, 'WS is maintained in the total population by between-group selection, despite its selective disadvantage within groups, exactly as envisioned by multi-level selection theory.' This is one possible interpretation of the facts, but it seems to me to go beyond the evidence presented by Rainey et al. We should note (as the Wilsons do not) that all surface mats collapse within a few days, whether or not they contain defectors. The regeneration of surface mats then depends on the establishment of a new population of WS individuals at the surface. These could emerge either by new mutations from the ancestral form, or from fragments of the collapsing WS mats. (It is not clear from the papers I have seen which of these usually occurs.) Either way, the Wilsons' description is incomplete. It implies that some WS 'groups' (the ones without defectors) survive indefinitely, while others fail. This is not the case. Even if a description in terms of group selection is formally valid, it does not (in my opinion) add much of value to the understanding of the phenomena. And if this is one of the best examples of group selection that its advocates can find, one cannot have much confidence in the others. (And indeed, some of the others, like the Wilsons' reference to the territorial behaviour of female lions, seem even worse. How can anyone sensibly discuss this without mentioning that the lionesses of a pride are usually closely related? [6, p. 37])

This is not to say that an account in terms of group selection will never provide useful insights into evolutionary processes. The evolution of disease organisms such as Myxomatosis seems to be one very plausible example. But the Wilsons' article does not persuade me that group selection, as distinct from inclusive fitness, is more than a minor wrinkle on the face of evolutionary theory.


[1] D. S. and E. O. Wilson: 'Rethinking the Theoretical Foundation of Sociobiology', Quarterly Review of Biology, December 2007, vol. 82. No.4, 327-348.

[2] J. Maynard Smith and E. Szathmary: The Origins of Life: from the birth of life to the origins of language, 1999

[3] P. B. and K. Rainey: 'Evolution of cooperation and conflict in experimental bacterial populations', Nature, 425, 2003, 72-4.

[4 P. B. and K. Rainey: 'Adaptive radiation in a heterogeneous environment', Nature, 394, 1998, 69-72.

[5] A. J. Spiers et al.: 'Adaptive divergence in experimental populations of Pseudomonas fluorescens. I: Genetic and phenotypic bases of Wrinkly Spreader fitness', Genetics, 161, 2002, 33-46.

[6] G. B. Schaller: The Serengeti Lion, 1972.

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