Population size mediates the contribution of high-rate and large-benefit mutations to parallel evolution

Martijn F. Schenk; Mark Zwart; Sungmin Hwang; Philip Ruelens; Edouard Severing; Joachim Krug; J. Arjan G. M. de Visser

doi:10.1038/s41559-022-01669-3

Population size mediates the contribution of high-rate and large-benefit mutations to parallel evolution

Martijn F. Schenk, Mark Zwart^* (Corresponding author), Sungmin Hwang, Philip Ruelens, Edouard Severing, Joachim Krug, J. Arjan G. M. de Visser

^*Corresponding author for this work

NIOO - Microbial Ecology (ME)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

Mutations with large fitness benefits and mutations occurring at high rates may both cause parallel evolution, but their contribution is predicted to depend on population size. Moreover, high-rate and large-benefit mutations may have different long-term adaptive consequences. We show that small and 100-fold larger bacterial populations evolve resistance to a β-lactam antibiotic by using similar numbers, but different types of mutations. Small populations frequently substitute similar high-rate structural variants and loss-of-function point mutations, including the deletion of a low-activity β-lactamase, and evolve modest resistance levels. Large populations more often use low-rate, large-benefit point mutations affecting the same targets, including mutations activating the β-lactamase and other gain-of-function mutations, leading to much higher resistance levels. Our results demonstrate the separation by clonal interference of mutation classes with divergent adaptive consequences, causing a shift from high-rate to large-benefit mutations with increases in population size.

Original language	English
Pages (from-to)	439-447
Number of pages	9
Journal	Nature Ecology and Evolution
Volume	6
Issue number	4
DOIs	https://doi.org/10.1038/s41559-022-01669-3
Publication status	Published - 2022

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Schenk et al 2022 AAMAccepted author manuscript, 3.69 MB

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title = "Population size mediates the contribution of high-rate and large-benefit mutations to parallel evolution",

abstract = "Mutations with large fitness benefits and mutations occurring at high rates may both cause parallel evolution, but their contribution is predicted to depend on population size. Moreover, high-rate and large-benefit mutations may have different long-term adaptive consequences. We show that small and 100-fold larger bacterial populations evolve resistance to a β-lactam antibiotic by using similar numbers, but different types of mutations. Small populations frequently substitute similar high-rate structural variants and loss-of-function point mutations, including the deletion of a low-activity β-lactamase, and evolve modest resistance levels. Large populations more often use low-rate, large-benefit point mutations affecting the same targets, including mutations activating the β-lactamase and other gain-of-function mutations, leading to much higher resistance levels. Our results demonstrate the separation by clonal interference of mutation classes with divergent adaptive consequences, causing a shift from high-rate to large-benefit mutations with increases in population size.",

author = "Schenk, {Martijn F.} and Mark Zwart and Sungmin Hwang and Philip Ruelens and Edouard Severing and Joachim Krug and {de Visser}, {J. Arjan G. M.}",

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AU - Schenk, Martijn F.

AU - Zwart, Mark

AU - Hwang, Sungmin

AU - Ruelens, Philip

AU - Severing, Edouard

AU - Krug, Joachim

AU - de Visser, J. Arjan G. M.

PY - 2022

Y1 - 2022

N2 - Mutations with large fitness benefits and mutations occurring at high rates may both cause parallel evolution, but their contribution is predicted to depend on population size. Moreover, high-rate and large-benefit mutations may have different long-term adaptive consequences. We show that small and 100-fold larger bacterial populations evolve resistance to a β-lactam antibiotic by using similar numbers, but different types of mutations. Small populations frequently substitute similar high-rate structural variants and loss-of-function point mutations, including the deletion of a low-activity β-lactamase, and evolve modest resistance levels. Large populations more often use low-rate, large-benefit point mutations affecting the same targets, including mutations activating the β-lactamase and other gain-of-function mutations, leading to much higher resistance levels. Our results demonstrate the separation by clonal interference of mutation classes with divergent adaptive consequences, causing a shift from high-rate to large-benefit mutations with increases in population size.

AB - Mutations with large fitness benefits and mutations occurring at high rates may both cause parallel evolution, but their contribution is predicted to depend on population size. Moreover, high-rate and large-benefit mutations may have different long-term adaptive consequences. We show that small and 100-fold larger bacterial populations evolve resistance to a β-lactam antibiotic by using similar numbers, but different types of mutations. Small populations frequently substitute similar high-rate structural variants and loss-of-function point mutations, including the deletion of a low-activity β-lactamase, and evolve modest resistance levels. Large populations more often use low-rate, large-benefit point mutations affecting the same targets, including mutations activating the β-lactamase and other gain-of-function mutations, leading to much higher resistance levels. Our results demonstrate the separation by clonal interference of mutation classes with divergent adaptive consequences, causing a shift from high-rate to large-benefit mutations with increases in population size.

U2 - 10.1038/s41559-022-01669-3

DO - 10.1038/s41559-022-01669-3

M3 - Article

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SP - 439

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JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 4

ER -

Population size mediates the contribution of high-rate and large-benefit mutations to parallel evolution

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