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The dynamics of molecular evolution over 60,000 generations

Author

Listed:
  • Benjamin H. Good

    (Harvard University
    FAS Center for Systems Biology, Harvard University
    Harvard University
    University of California Berkeley)

  • Michael J. McDonald

    (Harvard University
    FAS Center for Systems Biology, Harvard University
    Centre for Geometric Biology, School of Biological Sciences, Monash University)

  • Jeffrey E. Barrick

    (The University of Texas
    BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing)

  • Richard E. Lenski

    (BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing
    Michigan State University, East Lansing)

  • Michael M. Desai

    (Harvard University
    FAS Center for Systems Biology, Harvard University
    Harvard University)

Abstract

The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. However, it is difficult to observe these dynamics directly over long periods and across entire genomes. Here we analyse the dynamics of molecular evolution in twelve experimental populations of Escherichia coli, using whole-genome metagenomic sequencing at five hundred-generation intervals through sixty thousand generations. Although the rate of fitness gain declines over time, molecular evolution is characterized by signatures of rapid adaptation throughout the duration of the experiment, with multiple beneficial variants simultaneously competing for dominance in each population. Interactions between ecological and evolutionary processes play an important role, as long-term quasi-stable coexistence arises spontaneously in most populations, and evolution continues within each clade. We also present evidence that the targets of natural selection change over time, as epistasis and historical contingency alter the strength of selection on different genes. Together, these results show that long-term adaptation to a constant environment can be a more complex and dynamic process than is often assumed.

Suggested Citation

  • Benjamin H. Good & Michael J. McDonald & Jeffrey E. Barrick & Richard E. Lenski & Michael M. Desai, 2017. "The dynamics of molecular evolution over 60,000 generations," Nature, Nature, vol. 551(7678), pages 45-50, November.
  • Handle: RePEc:nat:nature:v:551:y:2017:i:7678:d:10.1038_nature24287
    DOI: 10.1038/nature24287
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    Citations

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    Cited by:

    1. Serhii Aif & Nico Appold & Lucas Kampman & Oskar Hallatschek & Jona Kayser, 2022. "Evolutionary rescue of resistant mutants is governed by a balance between radial expansion and selection in compact populations," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. N. Frazão & A. Konrad & M. Amicone & E. Seixas & D. Güleresi & M. Lässig & I. Gordo, 2022. "Two modes of evolution shape bacterial strain diversity in the mammalian gut for thousands of generations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Joao A. Ascensao & Kelly M. Wetmore & Benjamin H. Good & Adam P. Arkin & Oskar Hallatschek, 2023. "Quantifying the local adaptive landscape of a nascent bacterial community," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Ryo Mizuuchi & Taro Furubayashi & Norikazu Ichihashi, 2022. "Evolutionary transition from a single RNA replicator to a multiple replicator network," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Benjamin H. Good & Layton B. Rosenfeld, 2023. "Eco-evolutionary feedbacks in the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    6. Avik Mukherjee & Jade Ealy & Yanqing Huang & Nina Catherine Benites & Mark Polk & Markus Basan, 2023. "Coexisting ecotypes in long-term evolution emerged from interacting trade-offs," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    7. Piaopiao Chen & Jianzhi Zhang, 2024. "The loci of environmental adaptation in a model eukaryote," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Xueying C. Li & Lautaro Gandara & Måns Ekelöf & Kerstin Richter & Theodore Alexandrov & Justin Crocker, 2024. "Rapid response of fly populations to gene dosage across development and generations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Wen Wei & Wei-Chin Ho & Megan G. Behringer & Samuel F. Miller & George Bcharah & Michael Lynch, 2022. "Rapid evolution of mutation rate and spectrum in response to environmental and population-genetic challenges," Nature Communications, Nature, vol. 13(1), pages 1-10, December.

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