Robustness and Evolvability

doi:10.1016/j.tig.2010.06.002

Trends in Genetics

Volume 26, Issue 9, September 2010, Pages 406-414

https://doi.org/10.1016/j.tig.2010.06.002 Get rights and content

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.

Section snippets

Robustness affects evolvability in different ways

Biological organisms and computer programs are both encoded by a string of characters: DNA in organisms, binary code in programs. In biological systems, random mutations to DNA sequences are the fundamental source of long-term evolutionary adaptation. However, if one reduces a typical computer program to its binary sequence, making a random change to a single digit might literally have zero probability of improving the performance of the program [2]. But why? What makes biological systems

Post-mutation evolvability under high recombination rates

When a system is robust to mutations, selection does not prevent their accumulation. Later genetic or environmental changes might, however, cause changes to robustness that trigger the revelation of previously cryptic genetic variation. Cryptic genetic variation is abundant and ubiquitous 20, 21. The classic literature on cryptic genetic variation refers to high recombination: genetic assimilation, i.e. loss of crypticity, is envisaged to happen when many alleles, each cryptic on its own, are

Post-mutation evolvability under low recombination rates

One can envision the neutral region of a genotype space (Box 2, Box 3) as a ‘rug’ placed on a dusty floor [44], and each genotype present in a population as dust on that floor. Beyond the rug, genotypes are deleterious and swept away by selection, whereas under the rug, variation is hidden from selection (and is also free to accumulate further). Genetic robustness is determined, in part, by the size of the rug. In more extreme environments, or under the influence of an evolutionary capacitor,

Pre-mutation evolvability under low recombination rates

The dominant model for this category is the neutral network (Box 3) of phenotypically equivalent genotypes connected by single mutations. A population is typically spread out over some portion of this genotype space. Genetic robustness is defined as the probability that a mutation in an individual causes no change in phenotype; i.e. that the individual remains on the neutral network after a single mutational step in the genotype space. Different phenotypes are specified by different neutral

Pre-mutation evolvability under high recombination rates

Consider evolution in the same genotypic space, but now with significant recombination. Selection for robustness to recombination is now a strong force, with greater robustness to single mutations evolving as a correlated byproduct 75, 76, 77, 78. Selection for increased robustness within a given primary phenotype might constrain the range of genotypes and hence decrease evolvability in an asexual population [53]. But, although genetic diversity at single sites decreases with sex due to the

Concluding remarks

There are two somewhat separate literatures, both claiming that robustness promotes evolvability. One focuses largely on single genes and molecular phenotypes, uses the metaphor of neutral networks, and considers the effects of new mutations 10, 16, 51, 54, 56, 57, 58, 59, 60, 61. The other focuses on gene networks and morphological traits in multicellular organisms, and uses the Waddingtonian metaphors of canalization, cryptic genetic variation, and genetic assimilation 8, 17, 18, 20, 21, 23,

Acknowledgements

We thank Ben Wilson for technical help with Figure 1 and Jeremy Draghi, Etienne Rajon, Mark Siegal and three anonymous reviewers for helpful comments on the manuscript. This work was supported by the National Institutes of Health (R01GM076041). J.M. is a Pew Scholar in the Biomedical Sciences.

Glossary

Adaptive valley: when any mutational path between two high fitness genotypes or ‘adaptive peaks’ must pass through lower fitness mutational intermediates, the low fitness genotypes represent an adaptive valley.
Canalization and decanalization: canalization is biological robustness that evolves in the context of developmental processes [24]. Robustness or canalization is the extent to which phenotypes remain constant in the face of specified environmental and/or genetic perturbations. Decanalization

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