scholarly journals Cause and consequences of genome duplication in haploid yeast populations

2018 ◽  
Author(s):  
Kaitlin J. Fisher ◽  
Sean W. Buskirk ◽  
Ryan C. Vignogna ◽  
Daniel A. Marad ◽  
Gregory I. Lang
Keyword(s):  
Genome Duplication ◽  
Neutral Evolution ◽  
Phenotypic Evolution ◽  
Deleterious Mutations ◽  
Structural Variants ◽  
Laboratory Evolution ◽  
Fitness Advantage ◽  
Whole Genome Duplications ◽  
Genome Duplications

ABSTRACTWhole genome duplications (WGD) represent important evolutionary events that shape future adaptation. WGDs are known to have occurred in the lineages leading to plants, fungi, and vertebrates. Changes to ploidy level impact the rate and spectrum of beneficial mutations and thus the rate of adaptation. Laboratory evolution experiments initiated with haploid Saccharomyces cerevisiae cultures repeatedly experience WGD. We report recurrent genome duplication in 46 haploid yeast populations evolved for 4,000 generations. We find that WGD confers a fitness advantage, and this immediate fitness gain is accompanied by a shift in genomic and phenotypic evolution. The presence of ploidy-enriched targets of selection and structural variants reveals that autodiploids utilize adaptive paths inaccessible to haploids. We find that autodiploids accumulate recessive deleterious mutations, indicating an increased capacity for neutral evolution. Finally, we report that WGD results in a reduced adaptation rate, indicating a trade-off between immediate fitness gains and long term adaptability.

scholarly journals Genetic drift dominates genome-wide regulatory evolution following an ancient whole genome duplication in Atlantic salmon

2020 ◽  
Author(s):  
Jukka-Pekka Verta ◽  
Henry Barton ◽  
Victoria Pritchard ◽  
Craig Primmer
Keyword(s):  
Atlantic Salmon ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Regulatory Elements ◽  
Functional Redundancy ◽  
Neutral Evolution ◽  
Whole Genome ◽  
Regulatory Evolution ◽  
Whole Genome Duplications ◽  
Genome Duplications

AbstractWhole genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100-80 Mya. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained asymmetric regulatory evolution. Patterns of genetic diversity across natural populations inferred from re-sequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift.Significance statementRegulatory evolution following whole genome duplications (WGD) has been investigated at the gene expression level, but studies of the regulatory elements that control expression have been lacking. By investigating regulatory elements in the Atlantic salmon genome, which has undergone a whole genome duplication 100-80 million years ago, we discovered patterns suggesting that neutral divergence is the prevalent mode of regulatory element evolution post-WGD. Our results suggest mechanisms for explaining the prevalence of asymmetric gene expression evolution following whole genome duplication, as well as the mismatch between evolutionary rates in enhancers versus that of promoters.

scholarly journals The Role of Reticulate Evolution in Creating Innovation and Complexity

2012 ◽  
Vol 2012 ◽  
pp. 1-10 ◽  
Author(s):  
Kristen S. Swithers ◽  
Shannon M. Soucy ◽  
J. Peter Gogarten
Keyword(s):  
Metabolic Pathways ◽  
Driving Forces ◽  
Reticulate Evolution ◽  
Neutral Evolution ◽  
Ecological Niches ◽  
Eukaryotic Evolution ◽  
New Host ◽  
Whole Genome Duplications ◽  
Genome Duplications

Reticulate evolution encompasses processes that conflict with traditional Tree of Life efforts. These processes, horizontal gene transfer (HGT), gene and whole-genome duplications through allopolyploidization, are some of the main driving forces for generating innovation and complexity. HGT has a profound impact on prokaryotic and eukaryotic evolution. HGTs can lead to the invention of new metabolic pathways and the expansion and enhancement of previously existing pathways. It allows for organismal adaptation into new ecological niches and new host ranges. Although many HGTs appear to be selected for because they provide some benefit to their recipient lineage, other HGTs may be maintained by chance through random genetic drift. Moreover, some HGTs that may initially seem parasitic in nature can cause complexity to arise through pathways of neutral evolution. Another mechanism for generating innovation and complexity, occurring more frequently in eukaryotes than in prokaryotes, is gene and genome duplications, which often occur through allopolyploidizations. We discuss how these different evolutionary processes contribute to generating innovation and complexity.

scholarly journals Coregulation of tandem duplicate genes slows evolution of subfunctionalization in mammals

2015 ◽  
Author(s):  
Xun Lan ◽  
Jonathan K. Pritchard
Keyword(s):  
Gene Expression ◽  
Gene Dosage ◽  
Functional Adaptation ◽  
Small Scale ◽  
Loss Of Function ◽  
Whole Genome Duplications ◽  
Mouse Tissues ◽  
Genome Duplications ◽  
Key Factor

AbstractGene duplication is a fundamental process in genome evolution. However, most young duplicates are degraded into pseudogenes by loss-of-function mutations, and the factors that allow some duplicate pairs to survive long-term remain controversial. One class of models to explain duplicate retention invokes sub- or neofunctionalization, especially through evolution of gene expression, while other models focus on sharing of gene dosage. While studies of whole genome duplications tend to support dosage sharing, the primary mechanisms in mammals–where duplications are small-scale and thus disrupt dosage balance– are unclear. Using RNA-seq data from 46 human and 26 mouse tissues we find that sub-functionalization of expression evolves slowly, and is rare among duplicates that arose within the placental mammals. A major impediment to subfunctionalization is that tandem duplicates tend to be co-regulated by shared genomic elements, in contrast to the standard assumption of modularity of gene expression. Instead, consistent with the dosage-sharing hypothesis, most young duplicates are down-regulated to match expression of outgroup singleton genes. Our data suggest that dosage sharing of expression is a key factor in the initial survival of mammalian duplicates, followed by slower functional adaptation enabling long-term preservation.

scholarly journals Polyploidy and the Evolution of Complex Traits

2012 ◽  
Vol 2012 ◽  
pp. 1-12 ◽  
Author(s):  
Lukasz Huminiecki ◽  
Gavin C. Conant
Keyword(s):  
Complex Traits ◽  
Genome Duplication ◽  
Single Gene ◽  
Whole Genome ◽  
Gene Duplications ◽  
Evolutionary Potential ◽  
Evolutionary Transitions ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Modern Evolutionary Theory

We explore how whole-genome duplications (WGDs) may have given rise to complex innovations in cellular networks, innovations that could not have evolved through sequential single-gene duplications. We focus on two classical WGD events, one in bakers’ yeast and the other at the base of vertebrates (i.e., two rounds of whole-genome duplication: 2R-WGD). Two complex adaptations are discussed in detail: aerobic ethanol fermentation in yeast and the rewiring of the vertebrate developmental regulatory network through the 2R-WGD. These two examples, derived from diverged branches on the eukaryotic tree, boldly underline the evolutionary potential of WGD in facilitating major evolutionary transitions. We close by arguing that the evolutionary importance of WGD may require updating certain aspects of modern evolutionary theory, perhaps helping to synthesize a new evolutionary systems biology.

scholarly journals The Genetic Basis of Differential Autodiploidization in Evolving Yeast Populations

2021 ◽  
Author(s):  
Sudipta Tung ◽  
Christopher W Bakerlee ◽  
Angela M Phillips ◽  
Alex N Nguyen Nguyen Ba ◽  
Michael M Desai
Keyword(s):  
Genome Stability ◽  
Genetic Basis ◽  
Budding Yeast ◽  
Whole Genome ◽  
Laboratory Evolution ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Wild Strains ◽  
Potential Strategy ◽  
Functional Copy

Abstract Spontaneous whole-genome duplication, or autodiploidization, is a common route to adaptation in experimental evolution of haploid budding yeast populations. The rate at which autodiploids fix in these populations appears to vary across strain backgrounds, but the genetic basis of these differences remains poorly characterized. Here we show that the frequency of autodiploidization differs dramatically between two closely related laboratory strains of Saccharomyces cerevisiae, BY4741 and W303. To investigate the genetic basis of this difference, we crossed these strains to generate hundreds of unique F1 segregants and tested the tendency of each segregant to autodiplodize across hundreds of generations of laboratory evolution. We find that variants in the SSD1 gene are the primary genetic determinant of differences in autodiploidization. We then used multiple laboratory and wild strains of S. cerevisiae to show that clonal populations of strains with a functional copy of SSD1 autodiploidize more frequently in evolution experiments, while knocking out this gene or replacing it with the W303 allele reduces autodiploidization propensity across all genetic backgrounds tested. These results suggest a potential strategy for modifying rates of spontaneous whole-genome duplications in laboratory evolution experiments in haploid budding yeast. They may also have relevance to other settings in which eukaryotic genome stability plays an important role, such as biomanufacturing and the treatment of pathogenic fungal diseases and cancers.

scholarly journals ksrates: positioning whole-genome duplications relative to speciation events using rate-adjusted mixed paralog–ortholog KS distributions

2021 ◽  
Author(s):  
Cecilia Sensalari ◽  
Steven Maere ◽  
Rolf Lohaus
Keyword(s):  
Open Source Software ◽  
Genome Duplication ◽  
Synonymous Substitution ◽  
Whole Genome ◽  
Substitution Rates ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Command Line Tool ◽  
Synonymous Substitution Rates ◽  
User Friendly

Summary: To position ancient whole-genome duplication (WGD) events with respect to speciation events in a phylogeny, the KS values of WGD paralog pairs in a species of interest are often compared with the KS values of ortholog pairs between this species and other species. However, if the lineages involved exhibit different substitution rates, direct comparison of paralog and ortholog KS estimates can be misleading and result in phylogenetic misinterpretation of WGD signatures. Here we present ksrates, a user-friendly command-line tool to compare paralog and ortholog KS distributions derived from genomic or transcriptomic sequences. ksrates estimates differences in synonymous substitution rates among the lineages involved and generates an adjusted mixed plot of paralog and ortholog KS distributions that allows to assess the relative phylogenetic positioning of presumed WGD and speciation events. Availability and implementation: ksrates is open-source software implemented in Python 3 and as a Nextflow pipeline. The source code, Singularity and Docker containers, documentation and tutorial are available via https://github.com/VIB-PSB/ksrates.

scholarly journals Universal trends of post-duplication evolution revealed by the genomes of 13 Paramecium species sharing an ancestral whole-genome duplication

2019 ◽  
Author(s):  
Jean-Francois Gout ◽  
Parul Johri ◽  
Olivier Arnaiz ◽  
Thomas G. Doak ◽  
Simran Bhullar ◽  
...  
Keyword(s):  
Gene Loss ◽  
Genome Duplication ◽  
Model Organism ◽  
Whole Genome ◽  
Segmental Duplications ◽  
Gene Repertoire ◽  
Paramecium Tetraurelia ◽  
Selective Pressures ◽  
Whole Genome Duplications ◽  
Genome Duplications

AbstractWhole-Genome Duplications (WGDs) have shaped the gene repertoire of many eukaryotic lineages. The redundancy created by WGDs typically results in a phase of massive gene loss. However, some WGD-derived paralogs are maintained over long evolutionary periods and the relative contributions of different selective pressures to their maintenance is still debated. Previous studies have revealed a history of three successive WGDs in the lineage of the ciliate Paramecium tetraurelia and two of its sister species from the P. aurelia complex. Here, we report the genome sequence and analysis of 10 additional P. aurelia species and one additional outgroup, allowing us to track post-WGD evolution in 13 species that share a common ancestral WGD. We found similar biases in gene retention compatible with dosage constraints playing a major role opposing post-WGD gene loss across all 13 species. Interestingly we found that post-WGD gene loss was slower in Paramecium than in other species having experienced genome duplication, suggesting that the selective pressures against post-WGD gene loss are especially strong in Paramecium. We also report a lack of recent segmental duplications in Paramecium, which we interpret as additional evidence for strong selective pressures against individual genes dosage changes. Finally, we hope that this exceptional dataset of 13 species sharing an ancestral WGD and two closely related outgroup species will be a useful resource for future studies and will help establish Paramecium as a major model organism in the study of post-WGD evolution.

scholarly journals Selective constraints on coding sequences of nervous system genes are a major determinant of duplicate gene retention in vertebrates

2016 ◽  
Author(s):  
Julien Roux ◽  
Jialin Liu ◽  
Marc Robinson-Rechavi
Keyword(s):  
Nervous System ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Expression Patterns ◽  
Enrichment Analysis ◽  
Duplicate Genes ◽  
Whole Genome ◽  
Coding Sequences ◽  
Whole Genome Duplications ◽  
Genome Duplications

AbstractThe evolutionary history of vertebrates is marked by three ancient whole-genome duplications: two successive rounds in the ancestor of vertebrates, and a third one specific to teleost fishes. Biased loss of most duplicates enriched the genome for specific genes, such as slow evolving genes, but this selective retention process is not well understood. To understand what drives the long-term preservation of duplicate genes, we characterized duplicated genes in terms of their expression patterns. We used a new method of expression enrichment analysis, TopAnat, applied to in situ hybridization data from thousands of genes from zebrafish and mouse. We showed that the presence of expression in the nervous system is a good predictor of a higher rate of retention of duplicate genes after whole-genome duplication. Further analyses suggest that purifying selection against the toxic effects of misfolded or misinteracting proteins, which is particularly strong in non-renewing neural tissues, likely constrains the evolution of coding sequences of nervous system genes, leading indirectly to the preservation of duplicate genes after whole-genome duplication. Whole-genome duplications thus greatly contributed to the expansion of the toolkit of genes available for the evolution of profound novelties of the nervous system at the base of the vertebrate radiation.

scholarly journals Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

2021 ◽  
Author(s):  
Amber Harper ◽  
Luis Baudouin Gonzalez ◽  
Anna Schönauer ◽  
Ralf Janssen ◽  
Michael Seiter ◽  
...  
Keyword(s):  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Genetic Material ◽  
Gene Families ◽  
Comparative Approach ◽  
Whole Genome ◽  
Animal Evolution ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Horseshoe Crabs

Abstract Whole genome duplications have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss. It appears, however, that developmental genes such as homeobox genes, signalling pathway components and microRNAs are frequently retained as duplicates (so called ohnologs) following whole-genome duplication. These not only provide the best evidence for whole-genome duplication, but an opportunity to study its evolutionary consequences. Although these genes are well studied in the context of vertebrate whole-genome duplication, similar comparisons across the extant arachnopulmonate orders are patchy. We sequenced embryonic transcriptomes from two spider species and two amblypygid species and surveyed three important gene families, Hox, Wnt and frizzled, across these and twelve existing transcriptomic and genomic resources for chelicerates. We report extensive retention of putative ohnologs, further supporting the ancestral arachnopulmonate whole-genome duplication. We also found evidence of consistent evolutionary trajectories in Hox and Wnt gene repertoires across three of the six arachnopulmonate orders, with inter-order variation in the retention of specific paralogs. We identified variation between major clades in spiders and are better able to reconstruct the chronology of gene duplications and losses in spiders, amblypygids, and scorpions. These insights shed light on the evolution of the developmental toolkit in arachnopulmonates, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.

scholarly journals Natural selection can favor ratchet robustness over mutational robustness

2017 ◽  
Author(s):  
Yinghong Lan ◽  
Aaron Trout ◽  
Daniel Michael Weinreich ◽  
Christopher Scott Wylie
Keyword(s):  
Natural Selection ◽  
Natural Populations ◽  
Deleterious Mutations ◽  
Short Term ◽  
Mutational Robustness ◽  
Fundamental Interest ◽  
Fitness Advantage ◽  
Short And Long Term ◽  
Asexual Populations

AbstractThe vast majority of fitness-affecting mutations are deleterious. How natural populations evolve to cope is a question of fundamental interest. Previous studies have reported the evolution of mutational robustness, that is, natural selection favoring populations with less deleterious mutations. By definition, mutational robustness provides a short-term fitness advantage. However, this overlooks the fact that mutational robustness decreases finite asexual populations’ ability to purge recurrent deleterious mutations. Thus, mutational robustness also results in higher risk of long-term extinction by Muller’s ratchet. Here, we explore the tension between short- and long- term response to deleterious mutations. We first show that populations can resist the ratchet if either the selection coefficient or the ratio of beneficial to deleterious mutations increases as fitness declines. We designate these properties as ratchet robustness, which fundamentally reflects a negative feedback between mutation rate and the tendency to accumulate more mutations. We also find in simulations that populations can evolve ratchet robustness when challenged by deleterious mutations. We conclude that mutational robustness cannot be selected for in the long term, but it can be favored in the short-term, purely because of temporary fitness advantage. We also discuss other potential causes of mutational robustness in nature.

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