For the past two weeks I have been rather destructionist (is that a word), with my diatribe against kin selection. It seems to me that if you are going to tear down a structure and declare it not useful then you had better be willing to provide an alternative and explain why your alternative is a better choice. With that in mind, this week I will be talking about why I think the multilevel selection approach is the best, and possibly only legitimate, approach for studying social evolution.
In MLS theory the distinction between selection and the response to selection explicit. MLS theory is an outgrowth of quantitative genetics. The classic breeders equation, R=GP-1S, divides the response to selection, R, into the ecological process of selection, P-1S, and the mechanism of inheritance G. This is important because it also provides a guide to research. The reason that we did experimental studies of group selection in the laboratory is that it provided a means of studying G. That is, if we experimentally apply group selection did it cause a response to selection. The answer, of course is yes. I could go on with how this response was explored in some detail, but the point is these lab studies were explicitly designed to study G, the inheritance part of the breeders equation. On the other hand, the contextual analysis studies I have been talking about are primarily useful as phenotypic analyses, that can be applied to natural populations. Thus, we have a growing number of studies demonstrating that multilevel selection is quite common in nature. These studies tell us nothing about the inheritance, for the simple reason that the research is specifically designed to inform us about P-1S. The point is that experimental studies of inheritance are, both from a conceptual and practical perspective, very different from studies of selection. It is thus this distinction is not a minor triviality of the mathematics, it is a central and useful feature of the theory.
In MLS theory fitness is seen as a function of phenotype. In kin selection theory the modeled relationship is between fitness and gene. Efforts have been made to relax this, but ultimately the method is about the effect of single genes or at least very simple genetics on fitness. In MLS theory the modeled relationship is between fitness and phenotype. This is much more realistic. Phenotypes are what we measure in real populations. The relationship between phenotype and genotype is potentially very complex, and certainly not knowable in real field studies. The MLS approach acknowledges this reality, and as a result it is a method that can realistically be used to study natural selection in the wild. This is an area where kin selection simply fails.
In MLS theory the relationship between genotype and phenotype is acknowledged to be complex. In kin selection theory a single gene (or aspect of the genotype) is considered to affect both the individual trait (the cost) and the group trait (benefit). In MLS theory the group and individual trait are considered to be separate but correlated traits, and the genetics are expressed in the form of the G matrix. This allows for the simple system of kin selection (in which the correlation between expression at the two levels is 1), but allows for the possibility that they are not perfectly correlated. As an example, in a typical kin selection model you are either selfish or an altruist. However, if the correlation is not perfect, then you could get different degrees of “efficiency” for altruists. Then selection might favor the phenotype (note not genotype!) that provides the maximum altruism for the minimum cost. In the putative Haldane case, rather than sacrificing his life for his two brothers maybe he just has to cut off his arm. As importantly, as we discover added complexity in nature of inheritance the “inheritance” part of the equation can be modified as needed, either by modifying the G matrix, or when a clever enough theoretician comes along, replacing it with something new (Anyone want to take on coskewness tensors?).
MLS theory focuses on similarity regardless of cause. Hamilton’s rule in kin selection format:
can be reconstructed in MLS format in which case the equation comes down to:
this makes the point that any cause of variance among groups, or equivalently (because of the bizarre nature of statistics) any cause of similarity within groups can be on the right side of this equation. Kin selection, with its focus on shared genes as the cause of similarity falls short here. What else can cause similarity within groups? How about shared cultural heritage, or traditions? How about policing enforcing uniformity? This hugely broadens the range under which altruism can evolve.
The MLS approach is not obsessed with the evolution of altruism. The case where group and individual selection are acting in opposition is certainly interesting, but in kin selection it is the ONLY thing that is interesting. This is because it is an optimality approach and when they are acting in the same direction the equilibrium (fixation of the over all good gene) is trivial and uninteresting. Because the MLS approach measures selection as it is acting there is no need to focus solely on altruism. In general the word “altruism” is relatively rare in the MLS literature. It is an interesting sidelight, not the main focus of the research. This has lead to some interesting findings that are generally not appreciated outside of the MLS community. For example, individual selection interferes with group selection and is itself often ineffective due to indirect genetic effects. As a result, the overall response to simultaneous group selection and individual selection acting in concert is often less than simply the response to group selection acting along, and both are generally greater than the response to individual selection acting alone.
The MLS approach treats selection as a competing rates problem. Optimality approaches such as kin selection can at best tell us where a population “ought” to go, all things being equal. The problem is that all things are not equal, populations are not optimal, and there are a thousand contingencies keeping them away from simplistic optima. Because the MLS approach deals with the here and now, and how things are changing under the present conditions many of these problems go away. MLS approaches can be used to study stabilizing selection – either classic stabilizing selection at either the group or individual level, or stabilizing selection due to group and individual selection acting in opposition. However, note that I am not calling the stable equilibrium the “optimum”. In the example of group and individual selection acting in opposition the equilibrium point will be determined by a combination of the strength of selection at the two levels, the heritability of the group and individual level traits, and the genetic correlation between them.
I sum I think that the MLS is simply a better conceptual framework for thinking about social evolution. MLS theory fits firmly into the phenotypic approach, whereas kin selection theory, because of its focus on genes is basically incompatible with the phenotypic approach. MLS is by no means a mature theory, and there is much still to be done. But, heck that makes it exciting. The important point is that unlike kin selection theory, which is sadly stuck back in the 1960’s, MLS theory is an open ended field that is ripe to grow along with our increasing understanding of the subtleties of evolution.