Genetic variation in adaptability and pleiotropy in budding yeast

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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.

Data availability

The following data sets were generated

(2017) Data from: Genetic variation in adaptability and pleiotropy in budding yeast
Publicly available at the NCBI Sequence Read Archive (accession no. SRP102877).

https://www.ncbi.nlm.nih.gov/sra/?term=SRP102877

Article and author information

Author details

Elizabeth R Jerison

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

Competing interests
No competing interests declared.
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.
James Kameron Mitchell

Department of Physics, Harvard University, Cambridge, United States

Competing interests
No competing interests declared.
Joshua S Bloom

Department of Human Genetics, University of California, Los Angeles, Los Angeles, United States

Competing interests
No competing interests declared.
Leonid Kruglyak

Department of Human Genetics, University of California, Los Angeles, Los Angeles, United States

Competing interests
Leonid Kruglyak, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-8065-3057
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.

"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

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.