## Phase 3: Group selection by differential migration

Having taken a week off (blame it on Jason Wolf – he is the one who gave me a writing assignment!) it is time to get back to it. This week we turn to the final phase of Wright’s shifting balance process, phase three the phase of interdeme selection. In Wright’s view populations centered on high fitness peaks would tend to export more migrants than populations on lower fitness peaks, thus, high fitness populations are net exporters of migrants, whereas low fitness populations importers of migrants. Nice idea, but there are lots of reasons why it might not work.

One possible concern is whether or not group selection by differential migration will actually work. There are two lines of evidence that group selection by differential migration does indeed work, one experimental, and one theoretical.

The experimental study is a study by Wade and I (Wade and Goodnight 1991 Science 253: 1015). In this study we specifically examined whether selection by differential migration could result in a change in a response to selection. In this experiment we set up three pairs of metapopulations. Each pair consisted of two metapopulations of 50 subpopulations. In the first metapopulation we would count all of the adults, take the mean number of adults per subpopulation, and then calculate the relative fitness as:

were Ni is the population size of the ith subpopulation, N is the mean subpopulation size in the metapopulation and wi is relative fitness of the ith subpopulation. We would then perform selection by multiplying the founding population size (20 adults) by the relative fitness and taking that number of individuals to found the next generation. For example if the average population size at census time was 100 beetles, a population that produced 120 beetles would have a relative fitness of 1.2, and we would collect 24 offspring from the population. Similarly, one with a census number of 100 would have a relative fitness of 1, and produce 20 offspring, and one with a census size of 80 would have a relative fitness of 0.8 and produce 16 offspring. For each subpopulation the first 20 it produced would go back to found the next generation. If it produced more than 20 the remaining beetles went into a migrant pool. Thus, our first population would be founded with 20 from the parental population and 4 would go into the migrant pool. If the relative fitness was less than 20 then all of the beetles went back in to found the next generation, and the number was then made back up to 20 by sampling from the migrant pool. For example, in the third population, all 16 beetles from the parental population plus 4 from the migrant pool would be used to found the next generation.

In the paired population the same number of migrants was used, however, they were randomly chosen from the metapopulation without respect to fitness. The idea being to maintain the same level of migration, but to not have that migration correlated with fitness.

I should also add, so it doesn’t confuse things, there were three treatments, selection every generation, selection every other generation, and selection every third generation. In any case, we observed a substantial response to selection, and as usual, group selection is vindicated. It is, of course, standard fare that group selection is very effective, but prior to this study all group selection studies had been due to differential extinctions. This was the first to confirm that group selection by differential migration does indeed work.

The second piece of evidence is theoretical and provided by James Crow and his colleagues (Crow, Engels and Denniston 1990 Evolution 44: 233-247). In this paper they considered a situation in which there were two subpopulations, one fixed for a favorable combination of alleles at two or more loci, the second foxed for a less favorable combination. These combinations were separated by a fitness valley. They then asked what would happen if there was migration (either adult or zygote) between the two populations. The results of this model are nicely illustrated by their figure three.

In this figure the fitter gene subpopulation has a fitness of 1.2, and the less fit subpopulation has a starting fitness of 1.0. Migration from the fitter to the less fit subpopulation at first lowers the fitness of the subpopulation receiving migrants, but eventually leads to conversion over to the new fitness peak. From this they conclude that “The importance of Wright’s shifting-balance theory remains uncertain, but we believe that whatever weaknesses it may have are not in the third phase.”

Interestingly, Nick Barton, although he put a negative spin on it, confirmed Crows model of the efficacy of group selection by differential migration (Barton. 1992 Evolution 46: 551-557). He developed a model that was similar to Crows, but had migration be independent of fitness. That is he examined what happened if migration went from the less fit to the more fit subpopulation (among other things). In his conclusion he states:

“The striking results of Crow et al. (1990) are not due to selection in favor of a novel combination of genes, but rather reflect the power of gene flow over selection: the outcome is decided while the incoming alleles are at low frequency when the new well-adapted combination of genes has yet to appear.”

Barton goes on to conclude “Thus, while populations may well diversify through a “shifting balance,” it is difficult to see that this process leads to significant adaptation.”

I think one could rather conclude that his results confirm Crow et al.’s result that group selection by differential migration is very powerful, and in most cases it will overwhelm individual selection. Barton raises some important points. For example, Wright assumed that the most fit populations sent out the most migrants, however, relative fitness is a funny thing, and this certainly need not be the case. Indeed it is a bit of an unjustified leap of faith to believe that within population fitness in the form of increased survival and reproduction of individuals translates into higher among populations fitness in the form of increased emigration rate.

### 4 Responses to “Phase 3: Group selection by differential migration”

1. Joachim says:

George Williams and John Maynard Smith argued that between-group selection is usually not strong enough to overcome within-group selection. They thus framed the controversy in a way that the pertinent case is, where within- and between-group selection work in opposite directions, but between-group selection overcomes within-group selection.

To throw in cases where both forces work towards the same direction or where within-group selection is overcome by within-group drift rather that between-group selection confounds the controversy (or the controvertants), I guess.

2. Joachim;

Thanks for your comments. I tend not to think in terms of “altruism” — sort of a classic feature of multilevel selectionists, so I am not sure whether I agree with your or not. . .

Within the MLS community our models and experiments don’t typically assume that group and individual selection are in opposition. Indeed, in most experiments there is some sort of factorial structure that implies that in some treatments group and individual selection are necessarily acting in concert. Even if they are working in opposition the individual trait and the group trait are considered different traits, which is very different than the genic view where selection is acting directly on the genes and the correlation is constrained to -1.

As to the importance of drift: I think that most MLS models have been fighting the main stream beliefs, and thus set things up to be as bad as possible for group selection to be the dominant force. Small population size weakens individual selection, and makes drift more important, both features that favor group selection. Because small populations and drift favor group selection, most MLS models minimize the role of drift.

3. Joachim says:

Thanks for pointing this out. I nevertheless interpreted Wright’s group selection model (Wright S. 1945. “Tempo and Mode in Evolution: a critical review.” Ecology 26:415-419.)as inverted in comparison with later multilevel selection formulations. In Wright’s model, if the trait was altruism, selfish phenotypes would be overwhelmed by drift within groups, and the differential migration between groups is then a result of that within-group selection.

For an MLS example, the trait-group model of DS Wilson (1975) ignores drift within groups, lets the selfish individuals win within-group selection, but has them overwhelmed by variance in the average fitness between groups (given a cycle of groups dissolving in a panmictic population and randomly re-forming from that panmictic stage).

So I really see a difference between Wright’s model, where within-group drift and between-group migration rates work towards the same end, and MLS models where between-group statistics overwhelm within-group determinism.