Phenotypic plasticity as an adaptation to a functional trade-off

  1. Xiao Yi  Is a corresponding author
  2. Antony M Dean  Is a corresponding author
  1. University of Minnesota, United States

Abstract

We report the evolution of a phenotypically plastic behavior that circumvents the hardwired trade-off that exists when resources are partitioned between growth and motility in Escherichia coli. We propagated cultures in a cyclical environment, alternating between growth up to carrying capacity and selection for chemotaxis. Initial adaptations boosted overall swimming speed at the expense of growth. The effect of the trade-off was subsequently eased through a change in behavior; while individual cells reduced motility during exponential growth, the faction of the population that was motile increased as the carrying capacity was approached. This plastic behavior was produced by a single amino acid replacement in FliA, a regulatory protein central to the chemotaxis network. Our results illustrate how phenotypic plasticity potentiates evolvability by opening up new regions of the adaptive landscape.

Article and author information

Author details

  1. Xiao Yi

    Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, United States
    For correspondence
    xiaoyi8607@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4025-856X
  2. Antony M Dean

    Department od Ecology, Evolution and Behavior, University of Minnesota, St. Paul, United States
    For correspondence
    deanx024@umn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9546-7679

Funding

University of Minnesota (Research Support)

  • Xiao Yi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Wenying Shou, Fred Hutchinson Cancer Research Center, United States

Publication history

  1. Received: July 1, 2016
  2. Accepted: September 28, 2016
  3. Accepted Manuscript published: October 3, 2016 (version 1)
  4. Version of Record published: October 11, 2016 (version 2)
  5. Version of Record updated: October 13, 2016 (version 3)

Copyright

© 2016, Yi & Dean

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xiao Yi
  2. Antony M Dean
(2016)
Phenotypic plasticity as an adaptation to a functional trade-off
eLife 5:e19307.
https://doi.org/10.7554/eLife.19307

Further reading

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    Polygenic adaptation is thought to be ubiquitous, yet remains poorly understood. Here, we model this process analytically, in the plausible setting of a highly polygenic, quantitative trait that experiences a sudden shift in the fitness optimum. We show how the mean phenotype changes over time, depending on the effect sizes of loci that contribute to variance in the trait, and characterize the allele dynamics at these loci. Notably, we describe the two phases of the allele dynamics: The first is a rapid phase, in which directional selection introduces small frequency differences between alleles whose effects are aligned with or opposed to the shift, ultimately leading to small differences in their probability of fixation during a second, longer phase, governed by stabilizing selection. As we discuss, key results should hold in more general settings, and have important implications for efforts to identify the genetic basis of adaptation in humans and other species.

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    Cancer genomes exhibit surprisingly weak signatures of negative selection (Martincorena et al., 2017; Weghorn, 2017). This may be because selective pressures are relaxed or because genome-wide linkage prevents deleterious mutations from being removed (Hill-Robertson interference; Hill and Robertson, 1966). By stratifying tumors by their genome-wide mutational burden, we observe negative selection (dN/dS ~ 0.56) in low mutational burden tumors, while remaining cancers exhibit dN/dS ratios ~1. This suggests that most tumors do not remove deleterious passengers. To buffer against deleterious passengers, tumors upregulate heat shock pathways as their mutational burden increases. Finally, evolutionary modeling finds that Hill-Robertson interference alone can reproduce patterns of attenuated selection and estimates the total fitness cost of passengers to be 46% per cell on average. Collectively, our findings suggest that the lack of observed negative selection in most tumors is not due to relaxed selective pressures, but rather the inability of selection to remove deleterious mutations in the presence of genome-wide linkage.