Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations
Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 Saccharomyces cerevisiae populations (124 haploid and 81 diploid) for ~10,000 generations in three environments. We measured the d...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/63910 |
| _version_ | 1828168844560039936 |
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| author | Milo S Johnson Shreyas Gopalakrishnan Juhee Goyal Megan E Dillingham Christopher W Bakerlee Parris T Humphrey Tanush Jagdish Elizabeth R Jerison Katya Kosheleva Katherine R Lawrence Jiseon Min Alief Moulana Angela M Phillips Julia C Piper Ramya Purkanti Artur Rego-Costa Michael J McDonald Alex N Nguyen Ba Michael M Desai |
| author_facet | Milo S Johnson Shreyas Gopalakrishnan Juhee Goyal Megan E Dillingham Christopher W Bakerlee Parris T Humphrey Tanush Jagdish Elizabeth R Jerison Katya Kosheleva Katherine R Lawrence Jiseon Min Alief Moulana Angela M Phillips Julia C Piper Ramya Purkanti Artur Rego-Costa Michael J McDonald Alex N Nguyen Ba Michael M Desai |
| author_sort | Milo S Johnson |
| collection | DOAJ |
| description | Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 Saccharomyces cerevisiae populations (124 haploid and 81 diploid) for ~10,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in E. coli, we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions. |
| first_indexed | 2024-04-12T02:41:27Z |
| format | Article |
| id | doaj.art-e8d8f2f76fba43eeaf3f7eae82f045e8 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:41:27Z |
| publishDate | 2021-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e8d8f2f76fba43eeaf3f7eae82f045e82022-12-22T03:51:18ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.63910Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populationsMilo S Johnson0https://orcid.org/0000-0003-0169-2494Shreyas Gopalakrishnan1https://orcid.org/0000-0002-7243-0005Juhee Goyal2Megan E Dillingham3Christopher W Bakerlee4Parris T Humphrey5Tanush Jagdish6Elizabeth R Jerison7https://orcid.org/0000-0003-3793-8839Katya Kosheleva8Katherine R Lawrence9Jiseon Min10Alief Moulana11Angela M Phillips12Julia C Piper13Ramya Purkanti14Artur Rego-Costa15Michael J McDonald16Alex N Nguyen Ba17Michael M Desai18https://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 Molecular and Cellular Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; John A Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, United StatesQuantitative Biology Initiative, Harvard University, Cambridge, United States; Graduate Program in Systems, Synthetic, and Quantitative 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 Molecular and Cellular 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 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; Graduate Program in Systems, Synthetic, and Quantitative Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; Department of Physics, Harvard University, Cambridge, United States; Department of Applied Physics, Stanford University, Stanford, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; Department of Physics, 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, Massachusetts Institute of Technology, 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 Molecular and Cellular Biology, Harvard University, Cambridge, United States; John A Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; AeroLabs, Aeronaut Brewing Co, Somerville, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; The Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United StatesDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States; School of Biological Sciences, Monash University, Victoria, Monash, AustraliaDepartment 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 States; Department of Cell and Systems Biology, University of Toronto, Toronto, CanadaDepartment 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 StatesLaboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 Saccharomyces cerevisiae populations (124 haploid and 81 diploid) for ~10,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in E. coli, we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions.https://elifesciences.org/articles/63910experimental evolutionyeastdynamics of adaptation |
| spellingShingle | Milo S Johnson Shreyas Gopalakrishnan Juhee Goyal Megan E Dillingham Christopher W Bakerlee Parris T Humphrey Tanush Jagdish Elizabeth R Jerison Katya Kosheleva Katherine R Lawrence Jiseon Min Alief Moulana Angela M Phillips Julia C Piper Ramya Purkanti Artur Rego-Costa Michael J McDonald Alex N Nguyen Ba Michael M Desai Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations eLife experimental evolution yeast dynamics of adaptation |
| title | Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations |
| title_full | Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations |
| title_fullStr | Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations |
| title_full_unstemmed | Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations |
| title_short | Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations |
| title_sort | phenotypic and molecular evolution across 10 000 generations in laboratory budding yeast populations |
| topic | experimental evolution yeast dynamics of adaptation |
| url | https://elifesciences.org/articles/63910 |
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