High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast
Abstract
In rapidly adapting asexual populations, including many microbial pathogens and viruses, numerous mutant lineages often compete for dominance within the population. These complex evolutionary dynamics determine the outcomes of adaptation, but have been difficult to observe directly. Previous studies have used whole-genome sequencing to follow molecular adaptation; however, these methods have limited resolution in microbial populations. Here we introduce a renewable barcoding system to observe evolutionary dynamics at high resolution in laboratory budding yeast. We find nested patterns of interference and hitchhiking even at low frequencies. These events are driven by the continuous appearance of new mutations that modify the fates of existing lineages before they reach substantial frequencies. We observe how the distribution of fitness within the population changes over time, and find a travelling wave of adaptation that has been predicted by theory. We show that clonal competition creates a dynamical ‘rich-get-richer’ effect: fitness advantages that are acquired early in evolution drive clonal expansions, which increase the chances of acquiring future mutations. However, less-fit lineages also routinely leapfrog over strains of higher fitness. Finally, our results demonstrate that this combination of factors, which is not accounted for in existing models of evolutionary dynamics, is critical in determining themore »
- Authors:
-
- Harvard Univ., Cambridge, MA (United States)
- Harvard Univ., Cambridge, MA (United States); Massachusetts Inst. of Technology, Cambridge, MA (United States)
- Stanford Univ., CA (United States); Stony Brook Univ., NY (United States)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE; National Science Foundation (NSF); National Institutes of Health (NIH); Simons Foundation
- OSTI Identifier:
- 1596638
- Grant/Contract Number:
- AC02-76SF00515; DMS-1764269; HG008354; HL127522; 376196; DEB-1655960; GM104239
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 575; Journal Issue: 7783; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; experimental evolution; molecular evolution; population genetics
Citation Formats
Nguyen Ba, Alex N., Cvijović, Ivana, Rojas Echenique, José I., Lawrence, Katherine R., Rego-Costa, Artur, Liu, Xianan, Levy, Sasha F., and Desai, Michael M. High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. United States: N. p., 2019.
Web. doi:10.1038/s41586-019-1749-3.
Nguyen Ba, Alex N., Cvijović, Ivana, Rojas Echenique, José I., Lawrence, Katherine R., Rego-Costa, Artur, Liu, Xianan, Levy, Sasha F., & Desai, Michael M. High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. United States. https://doi.org/10.1038/s41586-019-1749-3
Nguyen Ba, Alex N., Cvijović, Ivana, Rojas Echenique, José I., Lawrence, Katherine R., Rego-Costa, Artur, Liu, Xianan, Levy, Sasha F., and Desai, Michael M. Wed .
"High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast". United States. https://doi.org/10.1038/s41586-019-1749-3. https://www.osti.gov/servlets/purl/1596638.
@article{osti_1596638,
title = {High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast},
author = {Nguyen Ba, Alex N. and Cvijović, Ivana and Rojas Echenique, José I. and Lawrence, Katherine R. and Rego-Costa, Artur and Liu, Xianan and Levy, Sasha F. and Desai, Michael M.},
abstractNote = {In rapidly adapting asexual populations, including many microbial pathogens and viruses, numerous mutant lineages often compete for dominance within the population. These complex evolutionary dynamics determine the outcomes of adaptation, but have been difficult to observe directly. Previous studies have used whole-genome sequencing to follow molecular adaptation; however, these methods have limited resolution in microbial populations. Here we introduce a renewable barcoding system to observe evolutionary dynamics at high resolution in laboratory budding yeast. We find nested patterns of interference and hitchhiking even at low frequencies. These events are driven by the continuous appearance of new mutations that modify the fates of existing lineages before they reach substantial frequencies. We observe how the distribution of fitness within the population changes over time, and find a travelling wave of adaptation that has been predicted by theory. We show that clonal competition creates a dynamical ‘rich-get-richer’ effect: fitness advantages that are acquired early in evolution drive clonal expansions, which increase the chances of acquiring future mutations. However, less-fit lineages also routinely leapfrog over strains of higher fitness. Finally, our results demonstrate that this combination of factors, which is not accounted for in existing models of evolutionary dynamics, is critical in determining the rate, predictability and molecular basis of adaptation.},
doi = {10.1038/s41586-019-1749-3},
journal = {Nature (London)},
number = 7783,
volume = 575,
place = {United States},
year = {Wed Nov 13 00:00:00 EST 2019},
month = {Wed Nov 13 00:00:00 EST 2019}
}
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