Trends in Genetics
ReviewRobustness and 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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