Last week I finished talking about gene interaction for at least a while. I hope I convinced you that assigning fitnesses to individual genes is a fools errand, both because in a world with interactions the assignment of fitnesses to individual alleles would be so context dependent as to be useless, and because it ends up being an NP hard problem that would require a computer larger than the universe to solve. At this point I want to turn to multilevel selection. I will start by talking about what I think is an important distinction that is rarely recognized, and ends up being a major contributor to the ongoing controversy that seems to surround multilevel selection.
It turns out that there two distinct approaches to the study of multilevel selection. One of these I will call the “adaptation” approach, and the other I will call the “evolutionary change” approach. (In Goodnight and Stevens (1997. Am. Nat. 150(Supplement): S59-S79) we called these the adapationist school and the genetical school.). If I come off biased it is because my thinking falls squarely in the evolutionary change school; however, both of these approaches are quite valid.
The adaptation approach is the most well known. In this approach an adaptation is identified, and plausible scenarios for its evolution are identified. The investigator then designs experiments and uses rules for deciding which of the plausible explanations is the most likely to be true. Some are eliminated due to the rules of science: any explanation involving a supernatural force (an intelligent designer or aliens) is automatically ruled out because such explanations cannot be subjected to scientific investigation, because science is only concerned with naturalistic explanations. Others must be eliminated by experimentation. For example, scientists have debated the origin of snakes, and why they are legless, since the 19th century. In recent years two major explanations have arisen for why snakes are legless. One is that snakes are of terrestrial origin, and lost their legs possibly as an adaptation to burrowing underground. The second, and currently more widely accepted is that they evolved from mosasaurs and are of marine origin. Under this model they lost their legs since they were fully aquatic. Distinguishing these two explanations is not trivial, and the debate is still on-going, with Vidal and Hedges (2004 Proc R. Soc Lond B 271:S226) using molecular phylogenetic evidence to argue for a terrestrial origin, and Lee (Biol Lett 2005 1:227), also using molecular phylogenetic evidence, arguing for a marine origin for snakes.
Two models for the evolution of leglessness in snakes. One is terrestrial, the other aquatic. The currently favored hypothesis is that ancient monitor lizards gave rise to mosasaurs, which in turn gave rise to snakes. In this hypothesis the garter snake sunning in your back yard is the descendent of a sea monster.
Unfortunately it is often impossible to eliminate all but one plausible naturalistic explanation. In this case it is necessary to establish rules for choosing among the available possibilities to decide on which is the most plausible. In the multilevel selection literature perhaps the most famous such rule is Williams’ principle of parsimony, which is worth quoting in full:
“In explaining adaptation, one should assume the adequacy of the simplest form of natural selection, that of alternative alleles in Mendelian populations, unless the evidence clearly shows that this theory does not suffice.” (G. C. Williams 1974. Adaptation and Natural Selection).
The important element that defines the adaptation approach is “in explaining adaptations”. Outside of subjects strictly associated with evolutionary theory nearly all of biology takes an adaption approach. That is, in physiology and anatomy it is taken as a given that a structure or behavior has an adaptive value, and the goal of most of the research is, in essence, determining what that adaptive value is. Within evolutionary biology, all of kin selection, game theory, some of multilevel selection, and all optimization theory in general falls into the realm of the adaptation approach. An excellent example of the adaptation approach using a multilevel selection is given in Wilson and Caldwell (Evolution 1981. 35:882).
In contrast the evolutionary change approach is used to study changes in populations resulting from ongoing evolutionary forces. It is usually applied to multilevel selection in two ways. First there is a long tradition of experiments in which selection is applied at the group level, and responses to that selection are observed. Second, contextual analysis has been used to study selection both theoretically and in the field. In the selection experiments group selection is applied as a treatment, and it is typically applied so that it in different treatments it may be acting in the same direction or in opposition to individual selection. Contextual analysis is a statistical analysis method that is basically a multiple regression selection analysis in which group and individual level traits are simultaneously included in the same analysis. Rather counter intuitively this system works to partition selection at multiple levels, a result that has been demonstrated both theoretically (e.g., Goodnight, Schwartz and Stevens 1992. Am. Nat. 140:743) and experimentally (e.g., Eldakar et al. 2010. Evolution 64: 3183). As with any selection analysis approach what is being measured is the covariance between group and individual level traits with relative fitness. This deserves further discussion, but in the interests of space we will leave discussion of the details for a later time. The important point is that what is measured is the change in phenotype within a generation due to selection.
The distinction between these two approaches is critical, and unfortunately not often appreciated. Most importantly, in the adaptive approach rules are needed to distinguish between different explanations, whereas such rules are of no use in the evolutionary change approach. This is the reason that Williams’ principle of parsimony is central to kin selection theory, but is almost never mentioned in papers using the evolutionary change approach. This is also why the kin selection theory essentially cares only about the evolution of altruism, whereas in MLS theory the evolution of altruism, which, if it is mentioned, is only mentioned as an afterthought. It really is stunning how little discussion of altruism there is in either the experimental group selection literature or in the contextual analysis literature.
To me one of the most confusing aspects of the multilevel selection vs kin selection controversy is that multilevel selection experiments are virtually never cited in kin selection discussions. More importantly, the central discovery of these studies: that group selection is more effective than expected because of genetically based interactions among individuals has never been incorporated into kin selection theory. This distinction between the adaptation approach and the evolutionary change approach may be an explanation. The evolutionary change approach is interested in process and interactions qualitatively affect the rate at which change occurs. In contrast, the adaptation approach is interested in endpoints. The rate at which those endpoints are achieved is of relatively little interest to this approach. Adaptationists should be careful, however. One thing that should be clear from my past blog posts on epistasis is that interactions can also change the endpoints.