Genetic background affects epistatic interactions between two beneficial mutations

Wang, Yinhua; Arenas, Carolina Díaz; Stoebel, Daniel M.; Cooper, Tim F.

doi:10.1098/rsbl.2012.0328

Cited by 49 publications

(47 citation statements)

References 23 publications

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“…Recent studies have found that epistatic interactions between beneficial mutations and their genetic backgrounds tend to become increasingly negative as the fitness of the genetic background increases (11)(12)(13)(14)(15)(16). If this relationship also holds across diverse recipient strains, we predict a negative relationship between the absolute fitness of a strain (measured as growth rate) and the benefit conferred by addition of a mutation.…”

Section: Fitter Recipient Strains Benefit Less From Introduced Mutatimentioning

confidence: 75%

“…15,35). We have extended this approach by estimating the effect of interactions between the broader genetic background and four mutations selected because they conferred a benefit in a population that was part of a long-term evolution experiment.…”

Section: Discussionmentioning

confidence: 99%

“…Epistasis plays a key role in many aspects of biology, including theories of speciation (2,3), the evolution and maintenance of sex (4,5), adaptation (6)(7)(8), and evolutionary contingency (9,10). Whereas early experimental studies focused on interactions between deletion or other knockout mutations, advances in genomic technologies now allow direct tests of interactions between spontaneously occurring beneficial mutations (11)(12)(13)(14)(15)(16). Studies that manipulate beneficial mutations have the potential to identify general patterns that may underlie some degree of predictability in adaptive evolutionary outcomes.…”

mentioning

confidence: 99%

“…Studies that manipulate beneficial mutations have the potential to identify general patterns that may underlie some degree of predictability in adaptive evolutionary outcomes. For example, interactions between beneficial mutations often follow a pattern of diminishing returns epistasis, such that the marginal benefit of additional mutations declines with the fitness of the recipient genotype (11)(12)(13)(14)(15)(16). Diminishing returns epistasis reflects a global interaction between mutations that interact at the level of fitness (16).…”

mentioning

confidence: 99%

“…Indeed, introgression experiments indicate the importance of the broader genetic background in determining the effect of specific genetic regions (reviewed in ref. 25), and even the interaction between two focal mutations depends strongly and perhaps unpredictably on the genetic background in which they are measured (15).…”

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confidence: 99%

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Benefit of transferred mutations is better predicted by the fitness of recipients than by their ecological or genetic relatedness

Wang

Arenas

Stoebel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The effect of a mutation depends on its interaction with the genetic background in which it is assessed. Studies in experimental systems have demonstrated that such interactions are common among beneficial mutations and often follow a pattern consistent with declining evolvability of more fit genotypes. However, these studies generally examine the consequences of interactions between a small number of focal mutations. It is not clear, therefore, that findings can be extrapolated to natural populations, where new mutations may be transferred between genetically divergent backgrounds. We build on work that examined interactions between four beneficial mutations selected in a laboratory-evolved population of Escherichia coli to test how they interact with the genomes of diverse natural isolates of the same species. We find that the fitness effect of transferred mutations depends weakly on the genetic and ecological similarity of recipient strains relative to the donor strain in which the mutations were selected. By contrast, mutation effects were strongly inversely correlated to the initial fitness of the recipient strain. That is, there was a pattern of diminishing returns whereby fit strains benefited proportionally less from an added mutation. Our results strengthen the view that the fitness of a strain can be a major determinant of its ability to adapt. They also support a role for barriers of transmission, rather than differential selection of transferred DNA, as an explanation of observed phylogenetically determined patterns of restricted recombination among E. coli strains.

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Section: Fitter Recipient Strains Benefit Less From Introduced Mutatimentioning

confidence: 75%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Benefit of transferred mutations is better predicted by the fitness of recipients than by their ecological or genetic relatedness

Wang

Arenas

Stoebel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Temperature affects the repeatability of evolution in the microbial eukaryote Tetrahymena thermophila

Tarkington

Zufall

2021

Ecology and Evolution

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Parallel genetic adaptation across environments differing in mode of growth or resource availability

2018

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Evolution experiments have demonstrated high levels of genetic parallelism between populations evolving in identical environments. However, natural populations evolve in complex environments that can vary in many ways, likely sharing some characteristics but not others. Here, we ask whether shared selection pressures drive parallel evolution across distinct environments. We addressed this question in experimentally evolved populations founded from a clone of the bacterium Burkholderia cenocepacia. These populations evolved for 90 days (approximately 600 generations) under all combinations of high or low carbon availability and selection for either planktonic or biofilm modes of growth. Populations that evolved in environments with shared selection pressures (either level of carbon availability or mode of growth) were more genetically similar to each other than populations from environments that shared neither characteristic. However, not all shared selection pressures led to parallel evolution. Genetic parallelism between low‐carbon biofilm and low‐carbon planktonic populations was very low despite shared selection for growth under low‐carbon conditions, suggesting that evolution in low‐carbon environments may generate stronger trade‐offs between biofilm and planktonic modes of growth. For all environments, a population's fitness in a particular environment was positively correlated with the genetic similarity between that population and the populations that evolved in that particular environment. Although genetic similarity was low between low‐carbon environments, overall, evolution in similar environments led to higher levels of genetic parallelism and that genetic parallelism, in turn, was correlated with fitness in a particular environment.

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Genetic background affects epistatic interactions between two beneficial mutations

Cited by 49 publications

References 23 publications

Benefit of transferred mutations is better predicted by the fitness of recipients than by their ecological or genetic relatedness

Benefit of transferred mutations is better predicted by the fitness of recipients than by their ecological or genetic relatedness

Temperature affects the repeatability of evolution in the microbial eukaryote Tetrahymena thermophila

Parallel genetic adaptation across environments differing in mode of growth or resource availability

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