Cooperation between phenotypic plasticity and genetic mutations can account for the cumulative selection in evolution

Abstract

We propose the cooperative model of phenotype-driven evolution, in which natural selection operates on a phenotype caused by both genetic and epigenetic factors. The conventional theory of evolutionary synthesis assumes that a phenotypic value (P) is the sum of genotypic value (G) and environmental deviation (E), P=G+E, where E is the fluctuations of the phenotype among individuals in the absence of environmental changes. In contrast, the cooperative model assumes that an evolution is triggered by an environmental change and individuals respond to the change by phenotypic plasticity (epigenetic changes). The phenotypic plasticity, while essentially qualitative, is denoted by a quantitative value F which is modeled as a normal random variable like E, but with a much larger variance. Thus, the fundamental equation of the cooperative model is given as P=G+F where F includes the effect of E. Computer simulations using a genetic algorithm demonstrated that the cooperative model realized much faster evolution than the evolutionary synthesis. This accelerated evolution was found to be due to the cumulative evolution made possible by a ratchet mechanism due to the epigenetic contribution to the phenotypic value. The cooperative model can well account for the phenomenon of genetic assimilation, which, in turn, suggests the mechanism of cumulative selection. The cooperative model may also serve as a theoretical basis to understand various ideas and phenomena of the phenotype-driven evolution such as genetic assimilation, the theory of facilitated phenotypic variation, and epigenetic inheritance over generations. In his Blind Watchmaker, Dawkins argues that evolution can be accelerated by the "cumulative selection" (Ref. 1, Chap. 3). For example, suppose that 10 genetic mutations (advan-tageous allele pairs) are required for the evolution of a certain trait. Even if mutations can be exchanged by genetic recombination, it is very difficult for the 10 mutations to accumulate in an individual. If, however, one mutation is not lost in subsequent recombinations and each recombination will only accumulate mutations, then the evolution is completed as soon as all the mutations have accumulated in an individual. According to Dawkins, this mechanism of the cumulative evolution drastically accelerates evolution so that most complicated organs such as the eye is possible within a certain geologic time scale. However, there seem to be no textbooks mentioning the concept of the cumulative evolution (e.g., Ref. 2), and the authors have also failed to find original papers mentioning it. It appears that this concept is completely ignored by experts. This may be an inevitable consequence of the fact that Dawkins himself does not explain by what mechanism and/or under what condition the cumulative evolution is possible. In the present study, we show that the cumulative evolution is impossible according to the conventional theory of evolutionary synthesis, which implies that the conventional theory cannot explain the evolution of complex phenotypes in a plausible time scale. We demonstrate , however, that the cumulative evolution can be made possible by a slight modification of the conventional theory.