Today I am speeding south on the Empire State in the morning and the Silver Star in the afternoon. I should be in Raleigh Durham for the Evolution meetings late this evening. For the uninitiated Amtrak trains have names that reflect where they are going. Thus, the famous Steve Goodman/Arlo Guthrie song, “City of New Orleans” is about the train that runs from Chicago to New Orleans. Finally, long distance trains have no internet, so this post is a bit sketchy. But, enough about trains, and on to phase one of Wright’s shifting balance. As I mentioned last week Wright identified three phases of his shifting balance process of how he thought populations might evolve on a complex adaptive landscape. The first of these phases is phase 1, the phase of random drift.
From an historical perspective, a pair of papers in Annual Reviews in 1984 (Carson and Templeton 1984 Ann. Rev 15:97-131, Barton and Charlesworth 1984 Ann. Rev. 15:133-164) are worth discussing. Although ostensibly about founder event speciation, they do a great job of laying out the state of the art for genetic drift in 1984. Taking the side that founder events (and by implication genetic drift) are relatively unimportant in evolution was Barton and Charlesworth, while Carson and Templeton attempted to defend founder event speciation.
Barton and Charlesworth’s points can be summarized in basically one sentence: Genetic drift and population bottlenecks reduce genetic variation, and honestly don’t change gene frequencies that much. In short genetic drift is unlikely to be important because it reduces a populations ability to respond to selection, and will cause the random loss of variation. From this perspective there is really no reason to give genetic drift an important role in evolution. In contrast Carson and Templeton argued that indeed there is something special about founder events, especially when there was epistasis, that they can drive a population to a new adaptive peak, and they should not be ignored. Here, however, is where they fell flat. In 1984 there was no theory on the effects of epistasis and genetic drift, or even a sense of how we should model it. The bottom line on these is that, in my view, Carson and Templeton were soundly defeated, not because they were wrong, but because they lacked any mathematical framework to use as scaffolding for their argument, whereas Barton and Charlesworth had the entire corpus of Fisher’s and Dobzhansky’s work to draw upon.
This pair of papers actually had quite an impact on me since they came out right after I finished my thesis, which had my original model of epistasis and founder events. I was sitting there with an unpublished manuscript on exactly the topic that would have completely changed the debate that these two pairs of authors were having (Goodnight 1987 Evolution 41:80-91).
What changed between 1984 and 1987 (actually 1995 – Goodnight 1995 Evolution 49: 501-511) was the development of formal models of the effect of genetic drift on epistatic variance. The important detail that Barton and Charlesworth did not have available to them was that the genetic variance components are a statistical property of a population, and they change as gene frequencies change. In the rather odd world of Fisher’s infinitesimal model even selection does not change gene frequencies, and as a result in Fisher-World© (OK, its not really copyrighted) it is completely valid to assume that additive genetic variance is a constant. However, Fisher also assumed that populations were infinitely large. If they are not infinitely large then gene frequencies DO change, and my models showed that on average these changes in gene frequency lead to an increase in the additive genetic variance. More importantly, Barton and Charlesworth also assumed that the average effects of alleles were constants, which is a valid assumption in Fisher-World. In my later models I showed that indeed there is only one way that additive genetic variance can increase following a population bottleneck. That is the only way to increase variance to change the average effects of alleles. Thus, in retrospect, the problem that Barton and Charlesworth had is that they were trying to apply Fisher-World reasoning to a situation in which it did not apply.
So, the way this applies to phase 1 of the shifting balance process is that it we need to acknowledge that drift is not just change in gene frequencies. Of course at a molecular level that is exactly what it is, but what we are interested in is the phenotype, and the quantitative genetic variance components. I would even go so far as to say it is not the increase in additive genetic variance that is particularly important. Of course, increasing the additive genetic variance increases the rate at which a population can respond to selection; however, getting to your destination a few generations early does not strike me as the stuff of the shifting balance process.
Instead, I think it is the shift in local average effects of alleles that are the interesting feature of drift with respect to the shifting balance process. What this means is that if two populations are isolated from each other then genetic drift can lead to a slight increase in additive genetic variance, but shifts in average effects of alleles that are different in the two populations. These shifts mean that the same allele is doing different things in different populations. It also means that selection acting on the same phenotype in the same manner in the two populations will favor different alleles. What is good in one population may be bad in another population.
Importantly, Wright, and Fisher, and even Barton and Charlesworth and Carson and Templeton did not have access to this. They considered average effects to be unchanging, and as a consequence missed one of the major features of drift in small populations. What these models tell us is that the population genetics of gene frequencies is very different from the quantitative genetics of phenotypes, and since evolution is about phenotypes in most cases it is the quantitative genetics that will be important.
Final note: Yes, of course Barton and Charlesworth, and all good quantitative geneticists know that average effects are a function of population characteristics and gene frequency, but this is not something that will normally enter their thinking or intuition.