scholarly journals Pervasive contingency and entrenchment in a billion years of Hsp90 evolution

2018 ◽  
Vol 115 (17) ◽  
pp. 4453-4458 ◽  
Author(s):  
Tyler N. Starr ◽  
Julia M. Flynn ◽  
Parul Mishra ◽  
Daniel N. A. Bolon ◽  
Joseph W. Thornton

Interactions among mutations within a protein have the potential to make molecular evolution contingent and irreversible, but the extent to which epistasis actually shaped historical evolutionary trajectories is unclear. To address this question, we experimentally measured how the fitness effects of historical sequence substitutions changed during the billion-year evolutionary history of the heat shock protein 90 (Hsp90) ATPase domain beginning from a deep eukaryotic ancestor to modern Saccharomyces cerevisiae. We found a pervasive influence of epistasis. Of 98 derived amino acid states that evolved along this lineage, about half compromise fitness when introduced into the reconstructed ancestral Hsp90. And the vast majority of ancestral states reduce fitness when introduced into the extant S. cerevisiae Hsp90. Overall, more than 75% of historical substitutions were contingent on permissive substitutions that rendered the derived state nondeleterious, became entrenched by subsequent restrictive substitutions that made the ancestral state deleterious, or both. This epistasis was primarily caused by specific interactions among sites rather than a general effect on the protein’s tolerance to mutation. Our results show that epistasis continually opened and closed windows of mutational opportunity over evolutionary timescales, producing histories and biological states that reflect the transient internal constraints imposed by the protein’s fleeting sequence states.

2017 ◽  
Author(s):  
Tyler N. Starr ◽  
Julia M. Flynn ◽  
Parul Mishra ◽  
Daniel N. A. Bolon ◽  
Joseph W. Thornton

AbstractInteractions among mutations within a protein have the potential to make molecular evolution contingent and irreversible, but the extent to which epistasis actually shaped historical evolutionary trajectories is unclear. We addressed this question by identifying all amino acid substitutions that occurred during the billion-year evolutionary history of the heat shock protein 90 (Hsp90) ATPase domain beginning from a deep eukaryotic ancestor to modern Saccharomyces cerevisiae and then precisely measuring their fitness effects when introduced into both extant and reconstructed ancestral Hsp90 proteins. We find a pervasive influence of epistasis: of 98 derived states that evolved during history, most were deleterious at times before they happened, and the vast majority also became subsequently entrenched, with the ancestral state becoming deleterious after its substitution. This epistasis was primarily caused by specific interactions among sites rather than a general permissive or restrictive effect on the protein’s tolerance to mutation. Our results show that epistasis continually opens and closes windows of mutational opportunity over evolutionary timescales, producing histories and biological states that reflect the transient internal constraints imposed by a protein’s fleeting sequence states.Significance statementWhen mutations within a protein change each other’s functional effects—a phenomenon called epistasis—the trajectories available to evolution at any moment in time depend on the specific set of changes that previously occurred in the protein. The extent to which epistasis has shaped historical evolutionary trajectories is unknown. Using a high-precision bulk fitness assay and ancestral protein reconstruction, we measured the fitness effects in ancestral and extant sequences of all historical substitutions that occurred during the billion-year trajectory of an essential protein. We found that most historical substitutions were contingent on prior epistatic substitutions and/or entrenched by subsequent changes. These results establish that epistasis caused widespread, consequential shifts in the site-specific fitness constraints that shaped the protein’s historical trajectory.


2006 ◽  
Vol 19 (2) ◽  
pp. 155 ◽  
Author(s):  
K. Watanabe ◽  
K. Kosuge ◽  
R. Shimamura ◽  
N. Konishi ◽  
K. Taniguchi

The intra-generic relationships of the Australian genus Calotis, with various chromosome base numbers from x = 8 to x = 4, were examined by the comparison of nucleotide sequences of the complete ITS region of nuclear rDNA and of the matK gene of chloroplast DNA. Within a monophyletic Calotis, four lineages were identified. Reconstruction of ancestral states suggests that the chromosome base number for Calotis is x = 8. Dysploidal reductions in chromosome base number from x = 8 to x = 7 and from x = 8 to x = 5 or 4 have occurred independently at least three times. Lower base numbers of x = 7, 5, and 4 are found predominantly in the arid and semi-arid zone species of Central and Western Australia. Total karyotypic length (genome size) is greater in perennials than in annuals within the genus Calotis. The elaborated pappus and surface structures of cypsela, and life form of species seem to be homoplasous with multiple origins in the evolutionary history of the lineage.


2021 ◽  
Author(s):  
Cedoljub Bundalovic-Torma ◽  
Darrell Desveaux ◽  
David S Guttman

A critical step in studying biological features (e.g., genetic variants, gene families, metabolic capabilities, or taxa) underlying traits or outcomes of interest is assessing their diversity and distribution. Accurate assessments of these patterns are essential for linking features to traits or outcomes and understanding their functional impact. Consequently, it is of crucial importance that the metrics employed for quantifying feature diversity can perform robustly under any evolutionary scenario. However, the standard metrics used for quantifying and comparing the distribution of features, such as prevalence, phylogenetic diversity, and related approaches, either do not take into consideration evolutionary history, or assume strictly vertical patterns of inheritance. Consequently, these approaches cannot accurately assess diversity for features that have undergone recombination or horizontal transfer. To address this issue, we have devised RecPD, a novel recombination-aware phylogenetic-diversity metric for measuring the distribution and diversity of features under all evolutionary scenarios. RecPD utilizes ancestral-state reconstruction to map the presence / absence of features onto ancestral nodes in a species tree, and then identifies potential recombination events in the evolutionary history of the feature. We also derive a number of related metrics from RecPD that can be used to assess and quantify evolutionary dynamics and correlation of feature evolutionary histories. We used simulation studies to show that RecPD reliably identifies evolutionary histories under diverse recombination and loss scenarios. We then apply RecPD in a real-world scenario in a preliminary study type III effector protein families secreted by the plant pathogenic bacterium Pseudomonas syringae and demonstrate that prevalence is an inadequate metric that obscures the potential impact of recombination. We believe RecPD will have broad utility for revealing and quantifying complex evolutionary processes for features at any biological level.


2015 ◽  
Author(s):  
Kerstin Howe ◽  
Philipp H Schiffer ◽  
Julia Zielinski ◽  
Thomas Wiehe ◽  
Gavin K Laird ◽  
...  

NACHT- and Leucine-Rich-Repeat-containing domain (NLR) proteins act as cytoplasmic sensors for pathogen- and danger-associated molecular patterns and are found throughout the plant and animal kingdoms. In addition to having a small set of conserved NLRs, the genomes in some animal lineages contain massive expansions of this gene family. One of these arose in fishes, after the creation of a gene fusion that combined the core NLR domains with another domain used for immune recognition, the PRY/SPRY or B30.2 domain. We have analysed the expanded NLR gene family in zebrafish, which contains 368 genes, and studied its evolutionary history. The encoded proteins share a defining overall structure, but individual domains show different evolutionary trajectories. Our results suggest gene conversion homogenizes NACHT and B30.2 domain sequences among different gene subfamilies, however, the functional implications of its action remains unclear. The majority of the genes are located on the long arm of chromosome 4, interspersed with several other large multi-gene families, including a new family encoding proteins with multiple tandem arrays of Zinc fingers. This suggests that chromosome 4 may be a hotspot for rapid evolutionary change in zebrafish.


2015 ◽  
Vol 112 (12) ◽  
pp. 3758-3763 ◽  
Author(s):  
Melanie J. Hopkins ◽  
Andrew B. Smith

How ecological and morphological diversity accrues over geological time has been much debated by paleobiologists. Evidence from the fossil record suggests that many clades reach maximal diversity early in their evolutionary history, followed by a decline in evolutionary rates as ecological space fills or due to internal constraints. Here, we apply recently developed methods for estimating rates of morphological evolution during the post-Paleozoic history of a major invertebrate clade, the Echinoidea. Contrary to expectation, rates of evolution were lowest during the initial phase of diversification following the Permo-Triassic mass extinction and increased over time. Furthermore, although several subclades show high initial rates and net decreases in rates of evolution, consistent with “early bursts” of morphological diversification, at more inclusive taxonomic levels, these bursts appear as episodic peaks. Peak rates coincided with major shifts in ecological morphology, primarily associated with innovations in feeding strategies. Despite having similar numbers of species in today’s oceans, regular echinoids have accrued far less morphological diversity than irregular echinoids due to lower intrinsic rates of morphological evolution and less morphological innovation, the latter indicative of constrained or bounded evolution. These results indicate that rates of evolution are extremely heterogenous through time and their interpretation depends on the temporal and taxonomic scale of analysis.


2015 ◽  
Vol 2015 ◽  
pp. 1-11 ◽  
Author(s):  
Billy W. Culver ◽  
Philip K. Morton

Understanding the mechanisms that drive acid-base regulation in organisms is important, especially for organisms in aquatic habitats that experience rapidly fluctuating pH conditions. Previous studies have shown that carbonic anhydrases (CAs), a family of zinc metalloenzymes, are responsible for acid-base regulation in many organisms. Through the use of phylogenetic tools, this present study attempts to elucidate the evolutionary history of the α-CA superfamily, with particular interest in the emerging model aquatic organism Daphnia pulex. We provide one of the most extensive phylogenies of the evolution of α-CAs, with the inclusion of 261 amino acid sequences across taxa ranging from Cnidarians to Homo sapiens. While the phylogeny supports most of our previous understanding on the relationship of how α-CAs have evolved, we find that, contrary to expectations, amino acid conservation with bacterial α-CAs supports the supposition that extracellular α-CAs are the ancestral state of animal α-CAs. Furthermore, we show that two cytosolic and one GPI-anchored α-CA in Daphnia genus have homologs in sister taxa that are possible candidate genes to study for acid-base regulation. In addition, we provide further support for previous findings of a high rate of gene duplication within Daphnia genus, as compared with other organisms.


2020 ◽  
Vol 37 (9) ◽  
pp. 2616-2629 ◽  
Author(s):  
Ming-Shan Wang ◽  
Sheng Wang ◽  
Yan Li ◽  
Yadvendradev Jhala ◽  
Mukesh Thakur ◽  
...  

Abstract Genetic introgression not only provides material for adaptive evolution but also confounds our understanding of evolutionary history. This is particularly true for canids, a species complex in which genome sequencing and analysis has revealed a complex history of admixture and introgression. Here, we sequence 19 new whole genomes from high-altitude Tibetan and Himalayan wolves and dogs and combine these into a larger data set of 166 whole canid genomes. Using these data, we explore the evolutionary history and adaptation of these and other canid lineages. We find that Tibetan and Himalayan wolves are closely related to each other, and that ∼39% of their nuclear genome is derived from an as-yet-unrecognized wolf-like lineage that is deeply diverged from living Holarctic wolves and dogs. The EPAS1 haplotype, which is present at high frequencies in Tibetan dog breeds and wolves and confers an adaptive advantage to animals living at high altitudes, was probably derived from this ancient lineage. Our study underscores the complexity of canid evolution and demonstrates how admixture and introgression can shape the evolutionary trajectories of species.


2019 ◽  
Author(s):  
Alex N. Salazar ◽  
Arthur R. Gorter de Vries ◽  
Marcel van den Broek ◽  
Nick Brouwers ◽  
Pilar de la Torre Cortès ◽  
...  

AbstractBackgroundThe lager brewing yeast,S. pastorianus, is a hybrid betweenS. cerevisiaeandS. eubayanuswith extensive chromosome aneuploidy.S. pastorianusis subdivided into Group 1 and Group 2 strains, where Group 2 strains have higher copy number and a larger degree of heterozygosity forS. cerevisiaechromosomes. As a result, Group 2 strains were hypothesized to have emerged from a hybridization event distinct from Group 1 strains. Current genome assemblies ofS. pastorianusstrains are incomplete and highly fragmented, limiting our ability to investigate their evolutionary history.ResultsTo fill this gap, we generated a chromosome-level genome assembly of theS. pastorianusstrain CBS 1483 using MinION sequencing and analysed the newly assembled subtelomeric regions and chromosome heterozygosity. To analyse the evolutionary history ofS. pastorianusstrains, we developed Alpaca: a method to compute sequence similarity between genomes without assuming linear evolution. Alpaca revealed high similarities between theS. cerevisiaesubgenomes of Group 1 and 2 strains, and marked differences from sequencedS. cerevisiae strains.ConclusionsOur findings suggest that Group 1 and Group 2 strains originated from a single hybridization involving a heterozygousS. cerevisiaestrain, followed by different evolutionary trajectories. The clear differences between both groups may originate from a severe population bottleneck caused by the isolation of the first pure cultures. Alpaca provides a computationally inexpensive method to analyse evolutionary relationships while considering non-linear evolution such as horizontal gene transfer and sexual reproduction, providing a complementary viewpoint beyond traditional phylogenetic approaches.


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