Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments
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.
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.
Metrics
-
- 980
- views
-
- 170
- downloads
-
- 4
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Evolutionary Biology
- Microbiology and Infectious Disease
Accurate estimation of the effects of mutations on SARS-CoV-2 viral fitness can inform public-health responses such as vaccine development and predicting the impact of a new variant; it can also illuminate biological mechanisms including those underlying the emergence of variants of concern. Recently, Lan et al. reported a model of SARS-CoV-2 secondary structure and its underlying dimethyl sulfate reactivity data (Lan et al., 2022). I investigated whether base reactivities and secondary structure models derived from them can explain some variability in the frequency of observing different nucleotide substitutions across millions of patient sequences in the SARS-CoV-2 phylogenetic tree. Nucleotide basepairing was compared to the estimated ‘mutational fitness’ of substitutions, a measurement of the difference between a substitution’s observed and expected frequency that is correlated with other estimates of viral fitness (Bloom and Neher, 2023). This comparison revealed that secondary structure is often predictive of substitution frequency, with significant decreases in substitution frequencies at basepaired positions. Focusing on the mutational fitness of C→U, the most common type of substitution, I describe C→U substitutions at basepaired positions that characterize major SARS-CoV-2 variants; such mutations may have a greater impact on fitness than appreciated when considering substitution frequency alone.
-
- Evolutionary Biology
Although fossil evidence suggests the existence of an early muscular system in the ancient cnidarian jellyfish from the early Cambrian Kuanchuanpu biota (ca. 535 Ma), south China, the mechanisms underlying the feeding and respiration of the early jellyfish are conjectural. Recently, the polyp inside the periderm of olivooids was demonstrated to be a calyx-like structure, most likely bearing short tentacles and bundles of coronal muscles at the edge of the calyx, thus presumably contributing to feeding and respiration. Here, we simulate the contraction and expansion of the microscopic periderm-bearing olivooid Quadrapyrgites via the fluid-structure interaction computational fluid dynamics (CFD) method to investigate their feeding and respiratory activities. The simulations show that the rate of water inhalation by the polyp subumbrella is positively correlated with the rate of contraction and expansion of the coronal muscles, consistent with the previous feeding and respiration hypothesis. The dynamic simulations also show that the frequent inhalation/exhalation of water through the periderm polyp expansion/contraction conducted by the muscular system of Quadrapyrgites most likely represents the ancestral feeding and respiration patterns of Cambrian sedentary medusozoans that predated the rhythmic jet-propelled swimming of the modern jellyfish. Most importantly for these Cambrian microscopic sedentary medusozoans, the increase of body size and stronger capacity of muscle contraction may have been indispensable in the stepwise evolution of active feeding and subsequent swimming in a higher flow (or higher Reynolds number) environment.