Robustness and evolvability

Abstract

Why isn't random variation always deleterious? Are there factors that sometimes make adaptation easier? Biological systems are extraordinarily robust to perturbation by mutations, recombination and the environment. It has been proposed that this robustness might make them more evolvable. Robustness to mutation allows genetic variation to accumulate in a cryptic state. Switching mechanisms known as evolutionary capacitors mean that the amount of heritable phenotypic variation available can be correlated to the degree of stress and hence to the novelty of the environment and remaining potential for adaptation. There have been two somewhat separate literatures relating robustness to evolvability. One has focused on molecular phenotypes and new mutations, the other on morphology and cryptic genetic variation. Here, we review both literatures, and show that the true distinction is whether recombination rates are high or low. In both cases, the evidence supports the claim that robustness promotes evolvability.

Figure 1

Interconnected nodes represent genotypes on a neutral network. Blue spheres represent genotypes present in the population and black spheres represent unoccupied nodes. (a) A neutral network with low intrinsic robustness has low spread and low evolvability. (b) A neutral network with high intrinsic robustness has its occupancy spread out across a larger portion of the network, gaining access to more potential variability. (c) In the presence of environmental perturbations some genotypes might generate the target phenotype more reliably than others, creating slight fitness differences. Selection for environmental robustness might hinder the spread of a population through a “nearly neutral network”. In our schematic, more environmentally robust genotypes (shown as higher) are more fit and so have higher occupancy than neighboring nodes.

Box 2 Figure I

Wright’s original adaptive landscape from 1932. Wright’s diagram illustrates the rapid increase in complexity of genotype space as number of loci increases. Conceptualizing a high-dimensional genotype space is very difficult. (Figure taken from [82]).