Mutational robustness changes during long-term adaptation in laboratory budding yeast populations

As an adapting population traverses the fitness landscape, its local neighborhood (i.e., the collection of fitness effects of single-step mutations) can change shape because of interactions with mutations acquired during evolution. These changes to the distribution of fitness effects can affect both...

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Main Authors: Milo S Johnson, Michael M Desai
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/76491
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author Milo S Johnson
Michael M Desai
author_facet Milo S Johnson
Michael M Desai
author_sort Milo S Johnson
collection DOAJ
description As an adapting population traverses the fitness landscape, its local neighborhood (i.e., the collection of fitness effects of single-step mutations) can change shape because of interactions with mutations acquired during evolution. These changes to the distribution of fitness effects can affect both the rate of adaptation and the accumulation of deleterious mutations. However, while numerous models of fitness landscapes have been proposed in the literature, empirical data on how this distribution changes during evolution remains limited. In this study, we directly measure how the fitness landscape neighborhood changes during laboratory adaptation. Using a barcode-based mutagenesis system, we measure the fitness effects of 91 specific gene disruption mutations in genetic backgrounds spanning 8000–10,000 generations of evolution in two constant environments. We find that the mean of the distribution of fitness effects decreases in one environment, indicating a reduction in mutational robustness, but does not change in the other. We show that these distribution-level patterns result from differences in the relative frequency of certain patterns of epistasis at the level of individual mutations, including fitness-correlated and idiosyncratic epistasis.
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spelling doaj.art-f471106a9d7b4dd69ac002a62e3925922022-12-22T03:50:48ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.76491Mutational robustness changes during long-term adaptation in laboratory budding yeast populationsMilo S Johnson0https://orcid.org/0000-0003-0169-2494Michael M Desai1https://orcid.org/0000-0002-9581-1150Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; Quantitative Biology Initiative, Harvard University, Cambridge, United States; NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; Quantitative Biology Initiative, Harvard University, Cambridge, United States; NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Cambridge, United States; Department of Physics, Harvard University, Cambridge, United StatesAs an adapting population traverses the fitness landscape, its local neighborhood (i.e., the collection of fitness effects of single-step mutations) can change shape because of interactions with mutations acquired during evolution. These changes to the distribution of fitness effects can affect both the rate of adaptation and the accumulation of deleterious mutations. However, while numerous models of fitness landscapes have been proposed in the literature, empirical data on how this distribution changes during evolution remains limited. In this study, we directly measure how the fitness landscape neighborhood changes during laboratory adaptation. Using a barcode-based mutagenesis system, we measure the fitness effects of 91 specific gene disruption mutations in genetic backgrounds spanning 8000–10,000 generations of evolution in two constant environments. We find that the mean of the distribution of fitness effects decreases in one environment, indicating a reduction in mutational robustness, but does not change in the other. We show that these distribution-level patterns result from differences in the relative frequency of certain patterns of epistasis at the level of individual mutations, including fitness-correlated and idiosyncratic epistasis.https://elifesciences.org/articles/76491epistasisrobustnessexperimental evolution
spellingShingle Milo S Johnson
Michael M Desai
Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
eLife
epistasis
robustness
experimental evolution
title Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
title_full Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
title_fullStr Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
title_full_unstemmed Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
title_short Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
title_sort mutational robustness changes during long term adaptation in laboratory budding yeast populations
topic epistasis
robustness
experimental evolution
url https://elifesciences.org/articles/76491
work_keys_str_mv AT milosjohnson mutationalrobustnesschangesduringlongtermadaptationinlaboratorybuddingyeastpopulations
AT michaelmdesai mutationalrobustnesschangesduringlongtermadaptationinlaboratorybuddingyeastpopulations