Beneficial mutations and the dynamics of adaptation in asexual populations

Sniegowski, Paul D.; Gerrish, Philip J.

doi:10.1098/rstb.2009.0290

Cited by 184 publications

(263 citation statements)

References 71 publications

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“…Various specific models have been developed to describe how advantageous mutations interact with each other and with other mutations. Models of clonal interference (CI) have been used to understand the evolution of bacteria as shown by Sniegowski & Gerrish (2010) in this themed issue. CI occurs when various asexual clones with different advantageous mutations compete against each other for fixation, for example in cells with different successful adaptations of metabolism to a new carbon source.…”

Section: Theories On the Population Genetics Of Mutationsmentioning

confidence: 99%

“…This is a controversial subject on which Charlesworth (2000) has made significant contributions. Models of the evolution of pathogenic microbes (Sniegowski & Gerrish 2010) and their mutations (Trindade et al 2010) are important for medical applications, such as optimizing the use of antibiotics to minimize resistance evolution and developing vaccines that might anticipate and neutralize simple evolutionary changes a pathogen is expected to produce. The wealth of data that can be obtained for these systems makes them attractive subjects for basic research on evolution.…”

Section: General Questions and Applicationsmentioning

confidence: 99%

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The population genetics of mutations: good, bad and indifferent

Loewe

Hill

2010

Phil. Trans. R. Soc. B

196

129

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Population genetics is fundamental to our understanding of evolution, and mutations are essential raw materials for evolution. In this introduction to more detailed papers that follow, we aim to provide an oversight of the field. We review current knowledge on mutation rates and their harmful and beneficial effects on fitness and then consider theories that predict the fate of individual mutations or the consequences of mutation accumulation for quantitative traits. Many advances in the past built on models that treat the evolution of mutations at each DNA site independently, neglecting linkage of sites on chromosomes and interactions of effects between sites (epistasis). We review work that addresses these limitations, to predict how mutations interfere with each other. An understanding of the population genetics of mutations of individual loci and of traits affected by many loci helps in addressing many fundamental and applied questions: for example, how do organisms adapt to changing environments, how did sex evolve, which DNA sequences are medically important, why do we age, which genetic processes can generate new species or drive endangered species to extinction, and how should policy on levels of potentially harmful mutagens introduced into the environment by humans be determined?

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Section: Theories On the Population Genetics Of Mutationsmentioning

confidence: 99%

Section: General Questions and Applicationsmentioning

confidence: 99%

The population genetics of mutations: good, bad and indifferent

Loewe

Hill

2010

Phil. Trans. R. Soc. B

196

129

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“…Consequently, little attention has been given to the role of the losers of adaptation, lineages that ultimately go extinct. Recent work has called into question the generality of the strong selection-weak mutation model of adaptation, where selective sweeps of beneficial mutations are brief and infrequent (Sniegowski and Gerrish 2010). Next-generation sequencing of entire adapting populations has demonstrated that multiple beneficial mutations compete for fixation within a common population (Lang et al 2013;Lieberman et al 2014), which leads to an increase in the average fitness of the ultimate winner (De Visser and Rozen 2006).…”

Section: Introductionmentioning

confidence: 99%

Here’s to the Losers: Evolvable Residents Accelerate the Evolution of High-Fitness Invaders

Gifford¹,

Toll-Riera²,

Kojadinovic³

et al. 2015

The American Naturalist

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Recent work has shown that evolvability plays a key role in determining the long-term population dynamics of asexual clones. However, simple considerations suggest that the evolvability of a focal lineage of bacteria should also be influenced by the evolvability of its competitors. First, evolvable competitors should accelerate evolution by impeding the fixation of the focal lineage through a clonal interference-like mechanism. Second, evolvable competitors should increase the strength of selection by rapidly degrading the environment, increasing selection for adaptive mutations. Here we tested these ideas by allowing a high-fitness clone of the bacterium Pseudomonas aeruginosa to invade populations of two low-fitness resident clones that differ in their evolvability. Both competition from mutations in the resident lineage and environmental degradation lead to faster adaptation in the invader through fixing single mutations with a greater fitness advantage. The results suggest that competition from mutations in both the successful invader and the unsuccessful resident shapes the adaptive trajectory of the invader through both direct competition and indirect environmental effects. Therefore, to predict evolutionary outcomes, it will be necessary to consider the evolvability of all members of the community and the effects of adaptation on the quality of the environment. This is particularly relevant to mixed microbial communities where lineages differ in their adaptive potential, a common feature of chronic infections. abstract: Recent work has shown that evolvability plays a key role in determining the long-term population dynamics of asexual clones. However, simple considerations suggest that the evolvability of a focal lineage of bacteria should also be influenced by the evolvability of its competitors. First, evolvable competitors should accelerate evolution by impeding the fixation of the focal lineage through a clonal interference-like mechanism. Second, evolvable competitors should increase the strength of selection by rapidly degrading the environment, increasing selection for adaptive mutations. Here we tested these ideas by allowing a high-fitness clone of the bacterium Pseudomonas aeruginosa to invade populations of two low-fitness resident clones that differ in their evolvability. Both competition from mutations in the resident lineage and environmental degradation lead to faster adaptation in the invader through fixing single mutations with a greater fitness advantage. The results suggest that competition from mutations in both the successful invader and the unsuccessful resident shapes the adaptive trajectory of the invader through both direct competition and indirect environmental effects. Therefore, to predict evolutionary outcomes, it will be necessary to consider the evolvability of all members of the community and the effects of adaptation on the quality of the environment. This is particularly relevant to mixed microbial communities where lineages differ in their adaptive potential, a...

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“…Biological considerations overwhelmingly support f D m D ) f B m B , so the left-hand side of (2.1) will most likely be positive. By some estimates [63][64][65][66][67][68], f B can be surprisingly high; however (i) this does not necessarily imply high values of f B m B [65] and (ii) it seems unlikely that f B m B would ever exceed f D m D , simply because the ways to damage a highly complex entity (such as a living organism) far outnumber the ways to improve it. In the very unlikely case that f B m B .…”

Section: Sufficient and Sufficient/necessary Conditionsmentioning

confidence: 99%

Genomic mutation rates that neutralize adaptive evolution and natural selection

Gerrish

Colato

Sniegowski

2013

J. R. Soc. Interface.

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When mutation rates are low, natural selection remains effective, and increasing the mutation rate can give rise to an increase in adaptation rate. When mutation rates are high to begin with, however, increasing the mutation rate may have a detrimental effect because of the overwhelming presence of deleterious mutations. Indeed, if mutation rates are high enough: (i) adaptive evolution may be neutralized, resulting in a zero (or negative) adaptation rate despite the continued availability of adaptive and/or compensatory mutations, or (ii) natural selection may be neutralized, because the fitness of lineages bearing adaptive and/or compensatory mutations-whether established or newly arising-is eroded by excessive mutation, causing such lineages to decline in frequency. We apply these two criteria to a standard model of asexual adaptive evolution and derive mathematical expressions-some new, some old in new guise-delineating the mutation rates under which either adaptive evolution or natural selection is neutralized. The expressions are simple and require no a priori knowledge of organism-and/or environment-specific parameters. Our discussion connects these results to each other and to previous theory, showing convergence or equivalence of the different results in most cases.

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Beneficial mutations and the dynamics of adaptation in asexual populations

Cited by 184 publications

References 71 publications

The population genetics of mutations: good, bad and indifferent

The population genetics of mutations: good, bad and indifferent

Here’s to the Losers: Evolvable Residents Accelerate the Evolution of High-Fitness Invaders

Genomic mutation rates that neutralize adaptive evolution and natural selection

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