In all of the previous discussions I have been talking about evolution through changes within species. However, when considering community selection there is another way that evolution can occur, that is evolution can occur through changes in species composition.
First off, I should mention that this is a classic case of listening to experiments. This was not a thought that occurred to me until after I read a pair of paper by Swenson and his colleagues (Swenson et al. 2000. P.N.A.S.97: 9110-9114; Swenson et al. 2000 Env. Microbiol. 2: 564-571). For that reason, and because the genetic school of group selection is quintessentially an experimental field, it makes sense to briefly describe one of their experiments.
In the experiment that I think is most compelling they went out a nearby garden and took a sample of soil. They took this soil, soaked it in water, and used the water to inoculate sterile soil. This soil was divided into 30 pots. Fifteen of these pots were assigned to the high selection line and fifteen were assigned to the low selection line (Yes, my big complaint with this experiment is the lack of replication). A number (about 50) of Arabidopsis seeds were planted into each pot. At the end of each “generation” the three pots with the highest (high selection line) or lowest (low selection line) were selected. The remaining 12 pots were discarded. In each line the soil from the three selected pots were mixed, water was added and the water was used to inoculate fifteen pots for the next generation. New Arabidopsis seeds from a stock population were again seeded into the soil. This process was continued for 16 generations. Note that the Arabidopsis were always drawn from a stock population, and as a result they could not evolve. Instead, Swenson and his colleagues were selecting for soil communities that either promoted or retarded the growth of the Arabidopsis plants.
As with all group selection type experiments, there was a significant response to selection (yea, I know it gets boring to say that, but remember that it was less than 20 years ago that Harrison and Hastings (1996 TR.E.E. 11: 180-183) said “ . . . extinction and recolonization have only a limited potential to create, or coexist with, strong genetic differentiation . . .. This implies that adaptive evolution is unlikely to occur by classic interdemic selection, a conclusion that has often been reached.”)
The interesting thing about this study is that they did not know what species were in the soil community. All they had was an extract of soil gathered from under some trees on campus. Nevertheless they got a substantial response to selection. It is likely true that some of the response to selection took place through genetic changes within the species in the communities, but it is more likely that the majority of the response to selection is due to change in species composition.
What appears to be happening here is that communities are varying in their species composition. Presumably there is little migration into the communities (but who knows with potentially airborne micro-organisms). Also the founding propagules were large: The small inoculum treatment had 0.6 grams of soil, which presumably had a LOT of micro-organisms. Thus, it is reasonable to speculate that every species was present in every experimental pot. What differed was the relative numbers of each species. Selection then presumably favored those communities that had high populations of species that promoted (or suppressed) plant growth. I have spoken with D. S. Wilson about this, and he told me that there were clear differences in the surface of the pots. For example, the pots that suppressed plant growth were often covered with algae.
In the Swenson study the communities were founded using a migrant pool model of migration. This considerably limits the modes by which adaptation can occur. As pointed out last time, in a migrant pool the interactions among species are randomized every generation. One presumes that the efficiency of community selection by species composition changes would be more efficient with a multispecies propagule pool. In that case favorable communities would have been transferred together, preserving the details of the community structure. Indeed, in a second experiment on community selection for pH of water they did use a multispecies propagule pool model. This second experiment was similar to the soil experiment, except that sterile pond water samples were inoculated with filtered pond water.
As usual there was a response to selection:
Unfortunately, since this is a very different system it is impossible to compare the two experiments for the effect of migration pattern.
Perhaps more important is the question of what is evolving here. In these experiments, as in all selection experiments, the selective agent is the investigator, and it is the investigator who decides what fitness is. In the case of the soil community experiments fitness was defined by plant growth, and yet the plants were not allowed to evolve. The soil community is evolving; however, at least in theory, this need not involve any genetic changes in the constituent species. If I may make a loose analogy, it seems that in this case the ecological “niches” are analogous to the loci of traditional genetics, and the micro-organism species are analogous to alleles. The analogy breaks down in the sense that in genetic systems there are exactly two alleles per locus, whereas in these communities it is not clear whether there it is the individual organism or the species that is the “allele”, and in either case there is not a fixed number of entities (alleles) per niche (locus). Interestingly, if we were somehow able to look at the constituent species, and pretend that evolution only occurred at the individual level we would (at least potentially) see no genetic changes in the community members, and conclude that there was no evolution going on. This emphasizes the absurdity of the reductionistic gene selection view. We have selection leading to a response to selection; however, because the changes are in species numbers rather than in genes, a gene selectionist would conclude that there was no evolution occurring.
Finally, the sad thing about this experiment is that it is a one-off experiment and as far as I am aware nobody has followed up on it. A molecular evolutionist could have a field day by screening the extracts for some measure of the community diversity; however, for what ever reason this experiment has not come to wide attention. In contrast people like myself are unlikely to have the skills or resources to be able to explore the changes taking place in a microbial community.