This week I want to finish up the discussion of indirect genetic effects and contextual traits by tying them back to the theme of this blog. Going way back to the early days (yes, next week this blog is one year old!), it is important to remember that the theme of this blog is that there is much to be gained by flipping our standard way of thinking about evolution on its head. That is, we typically think about evolution as something that happens to genes. In the shellfish jeans model of evolution it is genes that make phenotypes, to carry them forward to the next generation.http://www.lilikoijoy.com/2013/09/an-american-hometown-parade.html)
However, living things are complex systems, and as with any complex system there are multiple ways of looking at them. Each of the different ways of looking at a complex system is a way of simplifying it so that it is interpretable to the simple minds of humans, and as a result each will have strengths and weaknesses. I think it can be argued that the genic view has been useful in developing our understanding of how evolution works, in no small part because it simplifies the inheritance to the point of triviality. Haldane’s models of selection really helped us understand how selection works; however, it did so at the expense of anything resembling reality.
In contrast to the genic view I have been arguing that we should start thinking about phenotypes creating new phenotypes, and using genes as part of a “transition equation” that creates offspring phenotypes based on the characteristics of the parental phenotypes. At some level this is just another perspective from which to study evolution, and perhaps one that loses the simplistic view of genes as the center of evolution (Dare I follow Godfrey-Smith and call them rational agents?). What is gained from this view, however, is enough to make me, at least, think that it is more than “just another view”.
So far I have primarily focused on mechanical aspects of why the phenotypic view, as I call it, is in many respects preferable. Perhaps the greatest advantage is that evolution works on phenotypes, and in most cases it is phenotypic data we access to. It is a phenotypic perspective aligns with this reality. It always seemed to me rather irrational that we have this view of evolution based on change in a theoretical object that has little basis in reality (or as Pigliucci quoting Godfrey-Smith put it, genetic material is “a stuff not a discrete unit.”), which we are rarely in a position to measure, and when we do have access to things correlated with the genes (SNPs etc.) we more often then not discover that the “gene” is affected by a host of unidentified modifiers. How much more rational is it to construct a theory and a world view around the phenotype which is observable (or at least traits are observable), and that is the focus of selection and adaptation?
Nearly as great an advantage, however, is that the phenotype-to-phenotype transition equation is not constrained in the way that genes constrain our view to particulate inheritance. The transition equation can contain both Mendelian elements and continuous elements. The continuous elements can be either things that are truly continuous, such as culture, or they can be continuous approximations of underlying particulate traits, such as is used in quantitative genetics. This is actually more important than it appears at first blush. A theory of evolution based solely on changes in gene frequencies is simply inadequate given what we are beginning to learn about inheritance. Because we have this gene-based view of evolution we have had wildly difficult times incorporating even simple things like cytoplasmic inheritance, let alone complications such as epigenetics. Our usual approach is to study such things in isolation. Thus, we treat “cultural inheritance” as if it was somehow distinct and isolated from genic evolution. One need only look at the correlation between lactose tolerance in adults and the cultural use of cows to know that this isolation is simplistic. We also see extravagant claims that epigenetics are somehow distinct from “Darwinian” evolution. I am still looking for where Darwin discusses epigenetics in the Origin of Species.
The third advantage to the phenotypic approach is that the transition equation naturally incorporates various aspects of population structure. In the genic view mating and interaction structure are not easily incorporated since they don’t alter the structure of a gene. Instead they alter the effect of the gene on the phenotype, and how it affects heritability. It is this last area that has been the focus of recent blog posts. Starting with “measuring the heritability of contextual traits” and proceeding from there. Because the phenotype-to-phenotype transition equation is a means of predicting the distribution of phenotypes in the next generation it can easily be modified to include the effects of mating structure or interaction structure.
Perhaps the most dramatic distinction between the genic view and the phenotypic view comes with multilevel selection. Multilevel selection really is not particularly interesting from a genic perspective. If each gene is working for its own best interests in isolation from other genes then keeping track of selection structure is of little consequence or interest. Of course the down side to the simplistic genic view is that population structure does matter, and while using the genic perspective it is easy to make models that ignore population structure, they have precious little to do with muddy boots reality. From a phenotypic perspective, however, selection structure is important, and the level of selection will alter both the rate of adaptation and the qualitative nature of those adaptations. Rather satisfyingly, experimental results strongly support the idea that level of selection matters.
The point is that the things I have been discussing in this blog are wildly complicated from a genic view but naturally fall within the logic of the phenotypic view, thus, to reiterate a theme, while the genic view may be useful, it is perhaps time to move on and try to think about evolution from another perspective.
There is actually one more reason that the phenotypic perspective is useful. That is that there have been a number of controversies in evolutionary biology that have resisted easy analysis from the genic perspective. Many of these issues simply go away using a phenotypic approach. I will address some of these in the next few weeks. Hang on to your hat, it promises to be a wild ride.