Now that I have talked about how Wright thought evolution didn’t occur on adaptive landscapes, now it is time to talk about how he thought it did occur. The 7 assumptions and the adaptive topography were all basically background for his “shifting balance” process of evolution (Wright 1977 Evolution and Genetics of Populations. Vol. III. Experimental Results and Evolutionary Deductions. Univ. Chicago Press). To quickly summarize the previous few posts, Wright thought that the evolutionary possibilities could be visualized as an adaptive topography with fitness peaks and valleys.
Wright felt that very large or very small populations, or even a single medium sized population would not be able to navigate this topography, either because very large populations would be dominated by selection and unable to cross fitness valleys, or single very small populations would be so small and isolated that they would not be able to adequately explore the landscape. Instead, he thought that a metapopulation, or population of populations, would be the ideal population structure for evolution. (Of course, he did not use the term “metapopulation”: That term was coined by Levins, 1969 Bull. Entom. Soc. Am. 15: 237-240.) He basically thought that a medium size population would have a balance of drift and selection that it would allow the population to drift away from an adaptive peak and randomly explore the adaptive landscape. However, he also thought that a single population would be inadequate since the chance of that population actually coming under the selective domain of a new higher peak would be very small. Thus, he thought that the metapopulation structure with numerous moderate size populations was necessary since collectively they would be able to drift away from an adaptive peak and adequately explore the adaptive landscape.
The process he envisioned is his “shifting balance” process, which he imagined as a three phase process (I prefer calling it a process since the “theory” is whether or not the “process” is important. I also prefer SBP, because as an infant my daughter Sylvia’s nickname was Sylvia Bilvia Pilvia, or SBP for short.). The three phases he identified were:
(1) the phase of random drift. During this phase the subpopulations drift at random across the adaptive landscape. Drift is random with respect to fitness, thus, during this phase the populations are not constrained by selection, and can easily cross adaptive valleys.
(2) the phase of mass selection. During this phase the subpopulations come under the selective influence of local adaptive peaks and are driven by natural selection to climb the closest peak. Selection is a deterministic process that always drives the population “up hill” towards higher fitness, regardless of the height of the peak relative to other peaks.
(3) the phase of interdeme selection. During this phase the subpopulations that are on higher peaks are more successful, and as a result are net exporters of migrants, whereas those on lower peaks are less successful and net importers of migrants. Wright thought that this differential migration would effectively export successful adaptive gene combinations to other subpopulations, and eventually shift the balance of adaptation over to the new adaptive peak.
In Wright’s discussion it is clear that he considered these three processes to be occurring simultaneously within a metapopulation. Presumably any given subpopulation may at some times be dominated by random drift, with selection being a relatively weak force in that population, whereas other subpopulations may be under the influence of an adaptive peak and be more strongly influenced by selection. Finally, all subpopulations would be sending and receiving migrants. A subpopulation may be a net recipient of migrants while it is in an adaptive valley, but perhaps at a later point become a net exporter of migrants as it climbed a particularly good adaptive peak. It is this constant shifting of the balance of migration and selection from one peak to another that is the reason that Wright named this the “shifting balance” process.
It is clear why this process is so attractive to me, and many others. It is a theory that combines the stochastic processes of genetic drift with the deterministic processes of selection at multiple levels to lead to not only adaptation, but also to the evolution of novel solutions to the process of adaptation. That said there are more than a few reasons to be skeptical about the process (Coyne, Barton and Turelli 1997 Evolution 51: 643-671). Perhaps the most obvious is that the different phases of this proposed process require very different population sizes. For example, the drift phase will presumably be most effective if populations are small and isolated. In contrast, in phase two, the phase of mass selection, larger population sizes will make selection more effective, and random drift less important. Finally, phase three, the phase of interdeme selection is most effective with high migration rates. Thus, we have phase one requiring isolation and small population size; phase two requiring large population size; and phase 3 requiring high migration. This suggests that the three phases would be working at odds with each other, and is one of the main conceptual reasons that the shifting balance process is often discounted. My main thought on this is that, as we have seen in past posts, this is not the first time that we have seen theory being used to discredit the intuition of very smart experimentalists, and to repeat my favorite adage, when theory and experiment are in conflict, the theory is wrong.
As I have written elsewhere, we (Wade and Goodnight 1998 Evolution 52: 1537-1553.) think that it is premature to dismiss Wright’s shifting balance process based on intuition and parsimony reasoning. That said, Wright’s model is old, and it needs to be brought into the 21st century. What I will do over the next several weeks is discuss each of the phases in turn, and suggest ways in which discoveries made over the last 70 years can be incorporated and used to modify our understanding of the process originally proposed by Wright.