Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis

Organisms use a variety of strategies to adapt to their environments and maximize long-term growth potential, but quantitative characterization of the benefits conferred by the use of such strategies, as well as their impact on the whole population’s rate of growth, remains challenging. Here, we use...

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Main Authors: Guillaume Lambert, Edo Kussell
Format: Article
Language:English
Published: American Physical Society 2015-02-01
Series:Physical Review X
Online Access:http://doi.org/10.1103/PhysRevX.5.011016
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spelling doaj-d42cb634faee41d599003f27db11b47b2020-11-24T22:38:43ZengAmerican Physical SocietyPhysical Review X2160-33082015-02-015101101610.1103/PhysRevX.5.011016Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage AnalysisGuillaume LambertEdo KussellOrganisms use a variety of strategies to adapt to their environments and maximize long-term growth potential, but quantitative characterization of the benefits conferred by the use of such strategies, as well as their impact on the whole population’s rate of growth, remains challenging. Here, we use a path-integral framework that describes how selection acts on lineages—i.e., the life histories of individuals and their ancestors—to demonstrate that lineage-based measurements can be used to quantify the selective pressures acting on a population. We apply this analysis to Escherichia coli bacteria exposed to cyclical treatments of carbenicillin, an antibiotic that interferes with cell-wall synthesis and affects cells in an age-dependent manner. While the extensive characterization of the life history of thousands of cells is necessary to accurately extract the age-dependent selective pressures caused by carbenicillin, the same measurement can be recapitulated using lineage-based statistics of a single surviving cell. Population-wide evolutionary pressures can be extracted from the properties of the surviving lineages within a population, providing an alternative and efficient procedure to quantify the evolutionary forces acting on a population. Importantly, this approach is not limited to age-dependent selection, and the framework can be generalized to detect signatures of other trait-specific selection using lineage-based measurements. Our results establish a powerful way to study the evolutionary dynamics of life under selection and may be broadly useful in elucidating selective pressures driving the emergence of antibiotic resistance and the evolution of survival strategies in biological systems.http://doi.org/10.1103/PhysRevX.5.011016
collection DOAJ
language English
format Article
sources DOAJ
author Guillaume Lambert
Edo Kussell
spellingShingle Guillaume Lambert
Edo Kussell
Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
Physical Review X
author_facet Guillaume Lambert
Edo Kussell
author_sort Guillaume Lambert
title Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
title_short Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
title_full Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
title_fullStr Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
title_full_unstemmed Quantifying Selective Pressures Driving Bacterial Evolution Using Lineage Analysis
title_sort quantifying selective pressures driving bacterial evolution using lineage analysis
publisher American Physical Society
series Physical Review X
issn 2160-3308
publishDate 2015-02-01
description Organisms use a variety of strategies to adapt to their environments and maximize long-term growth potential, but quantitative characterization of the benefits conferred by the use of such strategies, as well as their impact on the whole population’s rate of growth, remains challenging. Here, we use a path-integral framework that describes how selection acts on lineages—i.e., the life histories of individuals and their ancestors—to demonstrate that lineage-based measurements can be used to quantify the selective pressures acting on a population. We apply this analysis to Escherichia coli bacteria exposed to cyclical treatments of carbenicillin, an antibiotic that interferes with cell-wall synthesis and affects cells in an age-dependent manner. While the extensive characterization of the life history of thousands of cells is necessary to accurately extract the age-dependent selective pressures caused by carbenicillin, the same measurement can be recapitulated using lineage-based statistics of a single surviving cell. Population-wide evolutionary pressures can be extracted from the properties of the surviving lineages within a population, providing an alternative and efficient procedure to quantify the evolutionary forces acting on a population. Importantly, this approach is not limited to age-dependent selection, and the framework can be generalized to detect signatures of other trait-specific selection using lineage-based measurements. Our results establish a powerful way to study the evolutionary dynamics of life under selection and may be broadly useful in elucidating selective pressures driving the emergence of antibiotic resistance and the evolution of survival strategies in biological systems.
url http://doi.org/10.1103/PhysRevX.5.011016
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