Gene expression noise can promote the fixation of beneficial mutations in fluctuating environments

Schmutzer, Michael; Wagner, Andreas

doi:10.1101/2020.02.13.947275

Cited by 7 publications

(7 citation statements)

References 83 publications

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“…2009), as suggested by recent experimental studies (Bódi et al. 2017; Schmutzer and Wagner 2020). However, this claim is in contradiction with classical theory that states that phenotypic noise always reduces the selection gradient (Lande 1975; Gavrilets and Hastings 1994; Wang and Zhang 2011; Mineta et al.…”

supporting

confidence: 52%

“…Because phenotypic noise increases the genotypic fitness of an organism far from the fitness optimum, it seems logical that it should facilitate adaptive evolution of the mean phenotype by increasing the fitness of beneficial mutations (Zhang et al 2009), as suggested by recent experimental studies (Bódi et al 2017;Schmutzer and Wagner 2020). However, this claim is in contradiction with classical theory that states that phenotypic noise always reduces the selection gradient (Lande 1975;Gavrilets and Hastings 1994;Wang and Zhang 2011;Mineta et al 2015;Tufto 2015).…”

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confidence: 96%

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Phenotypic noise and the cost of complexity

et al. 2020

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Experimental studies demonstrate the existence of phenotypic diversity despite constant genotype and environment. Theoretical models based on a single phenotypic character predict that during an adaptation event, phenotypic noise should be positively selected far from the fitness optimum because it increases the fitness of the genotype, and then be selected against when the population reaches the optimum. It is suggested that because of this fitness gain, phenotypic noise should promote adaptive evolution. However, it is unclear how the selective advantage of phenotypic noise is linked to the rate of evolution, and whether any advantage would hold for more realistic, multidimensional phenotypes. Indeed, complex organisms suffer a cost of complexity, where beneficial mutations become rarer as the number of phenotypic characters increases. Using a quantitative genetics approach, we first show that for a one-dimensional phenotype, phenotypic noise promotes adaptive evolution on plateaus of positive fitness, independently from the direct selective advantage on fitness. Second, we show that for multidimensional phenotypes, phenotypic noise evolves to a low-dimensional configuration, with elevated noise in the direction of the fitness optimum. Such a dimensionality reduction of the phenotypic noise promotes adaptive evolution and numerical simulations show that it reduces the cost of complexity.

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confidence: 52%

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confidence: 96%

Phenotypic noise and the cost of complexity

et al. 2020

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“…Second, somatic genotypic exploration allows selection to act on the potential of genotypes to produce non-heritable adaptive phenotypes, eventually rendering those phenotypes heritable. This makes somatic genotypic exploration akin to the genetic assimilation of plastic phenotypes triggered by environmental conditions [89][90][91][92] or by the stochasticity or "noise" of cellular processes [54,[93][94][95]. Within this context, the so-called "look-ahead effect" [54] is particularly relevant; in this model, phenotypic mutations caused by transcription or translation errors create potentially adaptive protein variants, offering a mechanism for channeling populations towards adaptive genotypes, as in our model.…”

Section: Evolutionary Implications Of Somatic Genotypic Explorationmentioning

confidence: 99%

The adaptive potential of non-heritable somatic mutations

Majic

2021

Preprint

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Non-heritable somatic mutations are typically associated with deleterious effects such as in cancer and senescence, so their role in adaptive evolution has received little attention. However, most somatic mutations are harmless and some even confer a fitness advantage to the organism carrying them. We hypothesized that heritable, germline genotypes that are likely to express an advantageous phenotype via non-heritable somatic mutation will have a selective advantage over other germline genotypes, and this advantage will channel evolving populations toward more fit germline genotypes, thus promoting adaptation. We tested this hypothesis by simulating evolving populations of developing organisms with an impermeable germline-soma separation navigating a minimal fitness landscape. The simulations revealed the conditions under which non-heritable somatic mutations promote adaptation. Specifically, this can occur when the somatic mutation supply is high, when only very few cells with the advantageous somatic mutation are required to increase organismal fitness, and when the somatic mutation also confers a selective advantage to cells with that mutation. We therefore provide proof-of-principle that non-heritable somatic mutations can promote adaptive evolution via a process we call somatic genotypic exploration. We discuss the biological plausibility of this phenomenon, as well as its evolutionary implications.

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“…As a result, we hypothesize that the plasticity of demographic noise holds more generally in selforganized systems (52), including colonies, biofilms, spatially-structured microbiomes, and solid cancer tumors, which would be interesting avenues for future study. Additionally, other phenotypic traits have been predicted to influence colony patterning and demographic noise and it would be interesting to test their influence on demographic noise in future work, including that of cell-cell and cell-substrate adhesion (53)(54)(55), cell orientations (32), cell elasticity (32), and variation in single cell growth rates (56,57) and lag times (58,59).…”

Section: Supplementary Section 25)mentioning

confidence: 99%

The mutability of demographic noise in microbial range expansions

Gralka

Duvernoy

et al. 2020

Preprint

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Demographic noise, the change in the composition of a population due to random birth and death events, is an important driving force in evolution because it reduces the efficacy of natural selection. Demographic noise is typically thought to be set by the population size and the environment, but recent experiments with microbial range expansions have revealed substantial strain-level differences in demographic noise under the same growth conditions. Many genetic and phenotypic differences exist between strains; to what extent do single mutations change the strength of demographic noise? To investigate this question, we developed a high-throughput method for measuring demographic noise in colonies without the need for genetic manipulation. By applying this method to 191 randomly-selected single gene deletion strains from the E. coli Keio collection, we find that a typical single gene deletion mutation decreases demographic noise by 8% (maximal decrease: 81%). We find that the strength of demographic noise is an emergent trait at the population level that can be predicted by colony-level traits but not cell-level traits. The observed differences in demographic noise from single gene deletions can increase the establishment probability of beneficial mutations by almost an order of magnitude higher than the wild type. Our results show that single mutations can substantially alter adaptation through their effects on demographic noise and suggest that demographic noise can be an evolvable phenotype of a population.

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Gene expression noise can promote the fixation of beneficial mutations in fluctuating environments

Cited by 7 publications

References 83 publications

Phenotypic noise and the cost of complexity

Phenotypic noise and the cost of complexity

The adaptive potential of non-heritable somatic mutations

The mutability of demographic noise in microbial range expansions

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