Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments
- Stanford University, United States
- Harvard University, United States
Abstract
Adaptation is driven by the selection for beneficial mutations that provide a fitness advantage in the specific environment in which a population is evolving. However, environments are rarely constant or predictable. When an organism well adapted to one environment finds itself in another, pleiotropic effects of mutations that made it well adapted to its former environment will affect its success. To better understand such pleiotropic effects, we evolved both haploid and diploid barcoded budding yeast populations in multiple environments, isolated adaptive clones, and then determined the fitness effects of adaptive mutations in “non-home” environments in which they were not selected. We find that pleiotropy is common, with most adaptive evolved lineages showing fitness effects in non-home environments. Consistent with other studies, we find that these pleiotropic effects are unpredictable: they are beneficial in some environments and deleterious in others. However, we do find that lineages with adaptive mutations in the same genes tend to show similar pleiotropic effects. We also find that ploidy influences the observed adaptive mutational spectra in a condition-specific fashion. In some conditions, haploids and diploids are selected with adaptive mutations in identical genes, while in others they accumulate mutations in almost completely disjoint sets of genes.
Data availability
All underlying sequencing data for both barcode sequencing and whole genome sequencing are available from the short read archive (SRA) under accession number PRJNA912754.
Article and author information
Author details
Funding
National Institute of General Medical Sciences (R35 GM131824)
- Gavin Sherlock
National Institute of General Medical Sciences (R35 GM118165)
- Dmitri A Petrov
National Institute of General Medical Sciences (R01 GM104239)
- Michael M Desai
National Science Foundation (PHY-1914916)
- Michael M Desai
National Science Foundation (DMS-1764269)
- Michael M Desai
National Science Foundation
- Milo S Johnson
National Institute of General Medical Sciences (R01 GM110275)
- Gavin Sherlock
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Detlef Weigel, Max Planck Institute for Biology Tübingen, Germany
Version history
- Preprint posted: March 1, 2023 (view preprint)
- Received: September 21, 2023
- Accepted: September 27, 2023
- Accepted Manuscript published: October 20, 2023 (version 1)
- Version of Record published: November 7, 2023 (version 2)
- Version of Record updated: November 8, 2023 (version 3)
Copyright
© 2023, Chen 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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Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments
eLife 12:e92899.
https://doi.org/10.7554/eLife.92899
Further reading
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The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.
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Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.
