How does evolution tune biological noise?

Abstract : Part of molecular and phenotypic differences between individual cells, between body parts, or between individuals can result from biological noise. This source of variation is becoming more and more apparent thanks to the recent advances in dynamic imaging and single-cell analysis. Some of these studies showed that the link between genotype and phenotype is not strictly deterministic. Mutations can change various statistical properties of a biochemical reaction, and thereby the probability of a trait outcome. The fact that they can modulate phenotypic noise brings up an intriguing question: how may selection act on these mutations? In this review, we approach this question by first covering the evidence that biological noise is under genetic control and therefore a substrate for evolution. We then sequentially inspect the possibilities of negative, neutral, and positive selection for mutations increasing biological noise. Finally, we hypothesize on the specific case of H2A.Z, which was shown to both buffer phenotypic noise and modulate transcriptional efficiency. The recent advances in dynamic imaging and single-cell studies have revealed the stochastic nature of biochemical reactions. Numerous factors are known to affect the degree of noise in these reactions, including temperature (Jo et al., 2005), drug treatment (Dar et al., 2014), age (Bahar et al., 2006) and, very importantly, genotypes (Raser and O'Shea, 2004; Levy and Siegal, 2008; Ansel et al., 2008; Hornung et al., 2012). If mutations can modulate a reaction without necessarily changing the average concentration of its product, then they do not fit in the traditional (often deterministic) view of genotype–phenotype control. Such mutations can change the probabilistic laws of single-cell traits, such as phenotypic noise, which may have important consequences at the multicellular level (Yvert, 2014). Noise has the property to increase disorder. In contrast, living systems are highly organized, developmental processes are under many constrains, and numerous phenotypic traits display robustness to stochastic variation. It is therefore unclear how optimization and control of noise can affect both fidelity and diversity. One way to apprehend this is to examine the mutations that were shown to increase or decrease noise levels. In this review, we first present evidence that noise is under genetic control. We then speculate on the ways by which natural selection acts on it. Finally, we hypothesize on the contribution of histone variant H2A.Z to noise evolution.
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Magali Richard, Gaël Yvert. How does evolution tune biological noise?. Frontiers in Genetics, Frontiers, 2014, ⟨10.3389/fgene.2014.00374⟩. ⟨ensl-01224442⟩

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