My life has gotten a bit hectic these days, so as usual a bit late, and perhaps a bit short. At this point I have gone through most of the basics that I wanted to talk about before getting into more speculative stuff, but I think that a few weeks of review and revisiting past posts is probably warranted. What I want to talk about for the next couple of weeks is something the difference between contextual traits and indirect genetic effects. I think that my past discussions on the difference have perhaps not been very clear, and I hate to say it, part of the problem may have been a bit of confusion on my part.
Turning first to contextual traits. It is important to remind ourselves that the classic breeder’s equation, R = GP-1S, divides evolution by selection into the ecological process of selection, and the heritable transmission represented by the G matrix. Contextual analysis, in its standard form, deals only with S. Thus if a trait is measured on the individual it is an individual trait, if it is measured on the context the individual finds itself in it is a contextual trait. The heritable (genetic?) basis is entirely irrelevant. The beauty of contextual analysis is that it is treats a trait that is measured on the context as if it were a trait of the individual. Thus if an individual is in a group of 16 individuals then it has the trait of “group size = 16”, if it is in a group that is 30% altruists, then it has the trait of “altruism level = 0.30”, and so on. Perhaps the correct way to think of it is that our individual is experiencing a group size of 16 or an altruism rate of 0.3.
In the early group selection days, people like Maynard-Smith insisted that group selection could only be invoked when groups were distinct entities that had clear borders. That is, groups were things you could walk around. Of course this becomes problematical when experimentalists examined the effects of migration (e.g., Wade 1982 Evolution 36, 945-61), or when you had group selection by differential migration (e.g., Wade and Goodnight 1991 Science 253, 1015). Contextual analysis allows us to resolve this issue easily. A contextual trait is a trait measured on the context. Classic Maynard-Smithian group selection is but one extreme of a continuum that ranges from group selection at one end to frequency dependent selection at the other extreme. Of course, this begs the questions: when is it group selection, and when is it frequency dependent selection. If the two are part of a continuum then where you draw the line is at some level arbitrary, and a matter of aesthetics rather than science. This also makes the interesting point that since the selective pressures on almost all traits are at some level dependent on the context the organism is found in, it suggests that pure individual selection, in which the fitness of an individual is solely dependent on its phenotype, and not at all influenced by the phenotype of its neighbors, is probably at least as rare as group selection acting by differential extinction and recolonization of whole groups. My guess is that viewing the evolution by natural selection outside of a multilevel selection perspective is simplistic, and frankly, wrong.
I should clarify one aspect of the frequency dependent selection issue. In mathematical modeling of selection there are frequency dependent models in which fitnesses change as gene frequencies change. Call this mathematical frequency dependence. In these models there is only one group, and as a result there can be no multilevel perspective. Importantly, these models cannot be used in (short-term) studies of real populations for the simple reason that gene frequencies rarely change fast enough to see this mathematical frequency dependence. To study frequency dependent selection in nature we need to find different populations that have different frequencies of the different phenotypes in different populations. This is statistical frequency dependence. I would argue that statistical, but not mathematical, frequency dependence should be studied as multilevel selection.
Another interesting point about contextual analysis: it comes from another field. The earliest reference in my endnote is (Przeworski 1974 Contextual models of political behavior. Polit. Method. 1, 27-61), although the more definitive reference is (Boyd and Iversen 1979 Contextual analysis: Concepts and statistical techniques. Wadsworth, Belmont, CA.). Since that time there have been a number of developments, and independent derivations of the technique. In 1987 Contextual analysis was introduced to the biological world (Heisler and Damuth 1987 Am. Nat. 130, 582). In 1996 contextual analysis was reinvented and called direct fitness, later called neighborhood modulated fitness (Taylor and Frank 1996 J. Theor. Biol 180, 27-37, arguably, Queller 1992 Evolution 46, 376-80.). In 2010 it was again rediscovered, although from a more genetic perspective, and labeled social selection (McGlothlin, Moorad , Wolf, and Brodie 2010 Evolution 64, 2558-74.). Bottom line: These are all the same thing. Contextual analysis has the precedence by nearly a decade over every other misbegotten term. Can we please just call everything by one name, and can it please be the name that crosses back to other scientific disciplines, and can it please be the one that respects precedence? All that those different things are contextual analysis. It is the only term that fulfills all those criteria, can we please just use contextual analysis. It is the correct term!
Finally, there is the interesting question of what is the correct trait. In our original contextual analysis papers (e.g., Goodnight, Schwartz, and Stevens 1992 Am. Nat. 140:743-761) we used the group mean of the trait, whereas McGlothlin et al. chose to use the mean of the group excluding the focal individual. Both of these make sense in the context that they were used. In our theoretical studies using the raw group mean considerably simplified the math, and made our message much clearer, whereas in the McGlothlin study they were considering social interactions explicitly, and it made sense to leave out the focal individual and only include those they interact with. Either and both of those are contextual traits, and as with any selection analysis the choice of which traits to include in the analysis depend on the situation.
OK, I will quit ranting. Next week I will move on to the indirect genetic effects I meant to get to this week.