Genetic variation in adaptability and pleiotropy in budding yeast

  1. Elizabeth R Jerison
  2. Sergey Kryazhimskiy
  3. James Kameron Mitchell
  4. Joshua S Bloom
  5. Leonid Kruglyak
  6. Michael M Desai  Is a corresponding author
  1. Harvard University, United States
  2. University of California, San Diego, United States
  3. University of California, Los Angeles, United States

Abstract

Evolution can favor organisms that are more adaptable, provided that genetic variation in adaptability exists. Here, we quantify this variation among 230 offspring of a cross between diverged yeast strains. We measure the adaptability of each offspring genotype, defined as its average rate of adaptation in a specific environmental condition, and analyze the heritability, predictability, and genetic basis of this trait. We find that initial genotype strongly affects adaptability and can alter the genetic basis of future evolution. Initial genotype also affects the pleiotropic consequences of adaptation for fitness in a different environment. This genetic variation in adaptability and pleiotropy is largely determined by initial fitness, according to a rule of declining adaptability with increasing initial fitness, but several individual QTLs also have a significant idiosyncratic role. Our results demonstrate that both adaptability and pleiotropy are complex traits, with extensive heritable differences arising from naturally occurring variation.

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The following data sets were generated

Article and author information

Author details

  1. Elizabeth R Jerison

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  2. Sergey Kryazhimskiy

    Section of Ecology, Behavior and Evolution, Division of Biological Sciences, University of California, San Diego, La Jolla, United States
    Competing interests
    No competing interests declared.
  3. James Kameron Mitchell

    Department of Physics, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  4. Joshua S Bloom

    Department of Human Genetics, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  5. Leonid Kruglyak

    Department of Human Genetics, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    Leonid Kruglyak, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8065-3057
  6. Michael M Desai

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    mdesai@oeb.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9581-1150

Funding

National Institutes of Health (R01GM102308)

  • Leonid Kruglyak

Simons Foundation (376196)

  • Michael M Desai

National Science Foundation (PHY 1313638)

  • Michael M Desai

Howard Hughes Medical Institute (Investigator)

  • Leonid Kruglyak

National Institutes of Health (R01GM104239)

  • Michael M Desai

National Science Foundation (Graduate Research Fellowship)

  • Elizabeth R Jerison

Burroughs Wellcome Fund (Career Award at the Scientific Interface)

  • Sergey Kryazhimskiy

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

Copyright

© 2017, Jerison et al.

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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https://doi.org/10.7554/eLife.27167

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