One of the striking results of the Wade group selection experiment is just how effective group selection was. Indeed, it was far more effective than anybody ever expected. On thinking about this Wade (and I as a hanger-on starting graduate student) a likely cause of this unexpected response quickly became clear. When Thomas Park did his work on the ecology of his population size strains of Tribolium confusum he concluded that the different population sizes were maintained by differences in cannibalism rate. From this we (ok, really Wade) speculated that the unexpected response to selection was due to group selection being able to act on interactions among individuals in general, or in the case of Tribolium on cannibalism rates.
This is an important point, because David Mertz told me (sadly, I doubt this is published) that they were unable to identify any nutritive advantage to cannibalism in standard high nutrient culture conditions typically used in the lab. If this is the case then cannibalism is a purely neutral trait at the individual level, but based on Park’s results, changes in cannibalism has huge consequences at the population level. Thus, we can speculate that the reason that group selection is so effective is that it can act on genetic effects (interactions among individuals) that have no effect on individual fitness, and simply cannot contribute to a response to selection at the individual level.
Not surprisingly, at some level we were re-inventing the wheel. It turns out that we were rediscovering something that plant breeders had known for a long time. That is, it has long been known that if you have a field of plants and you select the individuals with the greatest yield and plant up their seeds in the next generation you will frequently see a negative response to selection. That is if you select individuals for high yield, the yield per hectare will go down. The solution that plant breeders arrived at is “strain selection” in which they planted a plot of a particular cross, and chose plots that have the highest yield. In other words, they realized that if you want to increase yield per hectare, you should select on yield per hectare, not on yield per individual.
It also turns out that there are some very smart theoreticians in the plant-breeding world, and one of them was Bruce Griffing. Griffing decided to develop a quantitative genetic model that was done excruciatingly correctly, and as a result very confusingly. To get some idea of how detailed these models are, between 1981 and 1982 he published 10 papers on the subject in the journal of theoretical biology. Fortunately for us an abstract of this opus was published in 1977 (Griffing, 1977. Proceedings of the International Congress on Quantitative Genetics, August 16-21, 1976 ). (See Wolf, Brodie, Cheverud, Moore and Wade.1998 TREE13: 64-69. for a more modern approach to this problem)
Without going into the actual model, Griffing assumed that there were two traits, one which was direct effect of an individual on itself, and the other which was the indirect effect of an individual on others. Thus, for example, a direct effect trait might be the ability of a plant to absorb nutrients from the soil, and an indirect effect trait might be the extent to which a plant prevents neighbors from absorbing nutrients from the soil. The phenotype of an individual then is a combination of its ability to absorb nutrients, plus its neighbor’s ability to prevent it from absorbing nutrients.
He also assumed that there was a genetic correlation between them. In the example of our nutrient uptake, plants that were good at taking up nutrients would do so by taking from their neighbors, and thus suppressing their nutrient uptake. This makes logical sense. That is, the way a plant obtains more nutrients is to increase the root system, and to aggressively extract nutrients out of the soil. The nutrients have to come from somewhere, and where they come from is from nutrients their neighbors would otherwise have absorbed.
This is the problem with individual selection. Individual selection can only act on the direct effects. The indirect effects are neutral with respect to individual selection. Thus, selecting for the highest yielding plants selects for those plants that can most successfully extract nutrients are selected regardless of what effect they may have on neighboring plants. The next generation, when the selected offspring are planted together, the aggressive interactions prevail, and instead of getting an increase in yield, you get an increase in aggressiveness, and with it an overall lowering of yield. In other words, aggressiveness is a neutral trait evolves as a correlated response to selection, and this correlated response lowers the overall yield of the population. In still other words, you get a field of mean plants that spend their time beating on each other instead of doing their job.
In contrast group selection the aggressiveness is not neutral since selection is on the yield of the entire group. When selection is applied at the group level those fields that have the overall highest yield will be selected. This will favor a balance between the direct effects (ability to garner nutrients) and indirect effects (aggressiveness) that maximizes overall yield of the field or group. Notice that the yield of individual plants in this group are likely to be lower than could be attained by individual selection alone, but so will the aggressiveness towards other plants. In short it will be a typical compromise, where nobody is happy (that is, no sub-trait is maximized), but the overall outcome is best for all (total yield is maximized).
The point of this parable is that there is an important shift that takes place as selection moves from one level to another. Aggressiveness is not a trait that individual selection can act on and genetic variation for aggressiveness has no effect on individual fitness. As we move to the group level, aggressiveness does contribute to the response to group selection. Thus, this higher level of selection is drawing in components of variation that were not available to individual selection. In short group selection leads to a qualitatively different adaptation than will occur as a result of individual selection. That is also why the classical models failed so miserably. They assumed that variation in traits measured at the group level were simply composites (averages) of traits measured at the individual level. Instead, group level traits must be assumed to be different traits with a different genetic basis that simply cannot be extrapolated from individual level effects.
Take that Haystack Model! (Maynard Smith 1964. Nature 201: 1145-1147.) (http://www.sightswithin.com/Claude.Oscar.Monet/Page_3/)