Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations

Author:

Johnson Milo S123ORCID,Gopalakrishnan Shreyas1234ORCID,Goyal Juhee15,Dillingham Megan E26,Bakerlee Christopher W1234,Humphrey Parris T123,Jagdish Tanush1236,Jerison Elizabeth R178ORCID,Kosheleva Katya17,Lawrence Katherine R1239,Min Jiseon12345,Moulana Alief1,Phillips Angela M1,Piper Julia C110,Purkanti Ramya111,Rego-Costa Artur1,McDonald Michael J112,Nguyen Ba Alex N123713,Desai Michael M1237ORCID

Affiliation:

1. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States

2. Quantitative Biology Initiative, Harvard University, Cambridge, United States

3. NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Cambridge, United States

4. Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States

5. John A Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, United States

6. Graduate Program in Systems, Synthetic, and Quantitative Biology, Harvard University, Cambridge, United States

7. Department of Physics, Harvard University, Cambridge, United States

8. Department of Applied Physics, Stanford University, Stanford, United States

9. Department of Physics, Massachusetts Institute of Technology, Cambridge, United States

10. AeroLabs, Aeronaut Brewing Co, Somerville, United States

11. The Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany

12. School of Biological Sciences, Monash University, Victoria, Monash, Australia

13. Department of Cell and Systems Biology, University of Toronto, Toronto, Canada

Abstract

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.

Funder

National Science Foundation

Simons Foundation

Harvard University

National Defense Science and Engineering Graduate

Hertz Foundation

Department of Biotechnology , Ministry of Science and Technology

Australian Research Council

Natural Sciences and Engineering Research Council of Canada

National Institutes of Health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference74 articles.

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4. Escherichia coli cultures maintain stable subpopulation structure during long-term evolution;Behringer;PNAS,2018

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