Deciphering the genic basis of environmental adaptations by simultaneous forward and reverse genetics in<i>Saccharomyces cerevisiae</i>

Cj, MacLean; Bp, Metzger; Yang, Jiawen; Ho, W.; Moyers, Bryan A.; Zhang, J

doi:10.1101/087510

Cited by 3 publications

(9 citation statements)

References 72 publications

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“…cerevisiae was reconstructed using the single nucleotide polymorphism (SNP) data from Maclean et al 34 by the neighboring-joining method 35 with p-distance 36 implemented in MEGA 5.2.2 37 , and the matrix of pairwise phylogenetic distances was obtained by APE in R 38 .…”

Section: Mantel's Testmentioning

confidence: 99%

“…The rate of morphological evolution was calculated by the negative of this Spearman's correlation divided by genomic sequence dissimilarity (see below). Genomic sequence dissimilarity was calculated by the SNP density between two strains 34 . Ecological environment dissimilarity was set as 0 if two strains were sampled from the same ecological environment and 1 if sampled from different environments 34 .…”

Section: Mantel's Testmentioning

confidence: 99%

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Testing the neutral hypothesis of phenotypic evolution

Ohya

Zhang

2016

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It is generally accepted that a large fraction of genomic sequence variations within and between species are neutral or nearly so 1 . Whether the same is true for phenotypic variations is a central question in biology 2-7 . On the one hand, numerous phenotypic adaptations have been documented 2,8,9 and even Kimura, the champion of the neutral theory of molecular evolution, believed in widespread adaptive phenotypic evolution 1 . On the other hand, phenotypic studies are strongly biased toward traits that are likely to be adaptive 9 , contrasting genomic studies that are typically unbiased. It is thus desirable to test the neutral hypothesis of phenotypic evolution using traits irrespective of their potential involvement in adaptation. Here we present such a test for 210 morphological traits measured in multiple strains of the yeast Saccharomyces cerevisiae and two related species. Our test is based on the premise that, under neutrality, the rate of phenotypic evolution declines as the trait becomes more important to fitness, analogous to the neutral paradigm that functional genes evolve more slowly than functionless pseudogenes 10 .Neutrality is rejected in favor of adaptation if important traits evolve faster than less important ones, parallel to the demonstration of molecular adaptation when a functional gene evolves faster than pseudogenes. After controlling for the mutational size, we find faster evolution of more important morphological traits within and between species. By contrast, an analysis of 3466 yeast gene expression traits fails to reject neutrality. Thus, yeast morphological evolution is largely adaptive, but the same may not apply to other classes of phenotypes.Analogous to the neutral hypothesis of molecular evolution 1 , the neutral hypothesis of phenotypic evolution allows the presence of purifying selection; neutrality is rejected only when positive selection is invoked. Under the neutral hypothesis, compared with traits that are 3 relatively unimportant to fitness, relatively important traits should be subject to stronger purifying selection and evolve more slowly given the same speed of mutational input (Fig. 1a).However, if relatively important traits evolve faster than relatively unimportant traits, the neutral hypothesis would no longer hold and the only reasonable explanation would be stronger positive selection acting on relatively important traits than relatively unimportant ones ( Fig. 1b). This test of phenotypic neutrality differs from previous tests 3,4,[11][12][13][14][15] , which consider only one trait at a time and effectively require the intensity of positive selection to surpass that of purifying selection to reject neutrality. Because this requirement is sufficient but not necessary for demonstrating positive selection, it is replaced with the criterion of a positive correlation between trait importance and evolutionary rate to improve the power of the test (see Methods and Discussion).We first tested the neutral hypothesis of phenotypic evolution in a set of 210 morphologic...

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Section: Mantel's Testmentioning

confidence: 99%

Section: Mantel's Testmentioning

confidence: 99%

Testing the neutral hypothesis of phenotypic evolution

Ohya

Zhang

2016

Preprint

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“…While our study suggests the paucity of adaptive expression variations among the yeast strains studied, it does not exclude the possibility of a small fraction of genes whose expression variations are largely caused by adaptations. In fact, adaptive expressional differences among S. 21 cerevisiae strains have been suggested for some genes (23)(24)(25). It should be pointed out, however, that identifying an adaptive signal in the expression difference of a gene between two strains does not necessarily mean that their expression difference is entirely or even largely explained by adaptation.…”

Section: Discussionmentioning

confidence: 99%

“…We thus chose five other strains that have morphological data as their proxies. Each of the proxies is ecologically equivalent (with one exception) and, based on the established genome trees (20,21), phylogenetically close to the strain being replaced. The exception is the S. cerevisiae fruit juice strain DBVPG6040.…”

Section: The Transcriptome Tree Approximates the Genome Treementioning

confidence: 99%

“…The genome sequences of all S. cerevisae strains used here (Table S1) were obtained from a recently completed yeast population genomic study that sequenced 85 S. cerevisiae strains from a diverse array of ecological and geographic origins (21). S. cerevisiae genomic annotations were downloaded from SGD (22).…”

Section: Yeast Genome Sequences and Phylogenetic Analysismentioning

confidence: 99%

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Intra- and inter-specific variations of gene expression levels in yeast are largely neutral

Yang

Maclean

Park

et al. 2016

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It is commonly, although not universally, accepted that most intra-and inter-specific genome sequence variations are more or less neutral, whereas a large fraction of organism-level phenotypic variations are adaptive. Gene expression levels are molecular phenotypes that bridge the gap between genotypes and corresponding organism-level phenotypes. Yet, it is unknown whether natural variations in gene expression levels are mostly neutral or adaptive. Here we address this fundamental question by genome-wide profiling and comparison of gene expression levels in nine yeast strains belonging to three closely related Saccharomyces species and originating from five different ecological environments. We find that the transcriptome-based clustering of the nine strains approximates the genome sequence-based phylogeny irrespective of their ecological environments. Remarkably, only ~0.5% of genes exhibit similar expression levels among strains from a common ecological environment, no greater than that among strains with comparable phylogenetic relationships but different environments. These and other observations strongly suggest that most intra-and inter-specific variations in yeast gene expression levels result from the accumulation of random mutations rather than environmental adaptations. This finding has profound implications for understanding the driving force of gene expression evolution, genetic basis of phenotypic adaptation, and general role of stochasticity in evolution. 3 SIGNIFICANCEIt is believed that most genomic variations within and between species are more or less neutral, while a large fraction of organism-level phenotypic variations are adaptive. Gene expression bridges the gap between genome sequences and organismal phenotypes, but it is unclear whether variations in gene expression levels are mostly neutral or adaptive. By quantifying the genome-wide gene expression levels in nine yeast strains whose phylogenetic relationships mismatch the relationships of their ecological environments, we find that transcriptome variations can be explained by the accumulation of random mutations but not environmental adaptations. This finding has important implications for understanding the driving force of gene expression evolution, genetic basis of phenotypic adaptation, and general role of stochasticity in evolution.

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Evolutionary Dynamics of Regulatory Changes Underlying Gene Expression Divergence among Saccharomyces Species

Metzger

Wittkopp

Coolon

2017

Genome Biology and Evolution

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Heritable changes in gene expression are important contributors to phenotypic differences within and between species and are caused by mutations in cis-regulatory elements and trans-regulatory factors. Although previous work has suggested that cis-regulatory differences preferentially accumulate with time, technical restrictions to closely related species and limited comparisons have made this observation difficult to test. To address this problem, we used allele-specific RNA-seq data from Saccharomyces species and hybrids to expand both the evolutionary timescale and number of species in which the evolution of regulatory divergence has been investigated. We find that as sequence divergence increases, cis-regulatory differences do indeed become the dominant type of regulatory difference between species, ultimately becoming a better predictor of expression divergence than trans-regulatory divergence. When both cis- and trans-regulatory differences accumulate for the same gene, they more often have effects in opposite directions than in the same direction, indicating widespread compensatory changes underlying the evolution of gene expression. The frequency of compensatory changes within and between species and the magnitude of effect for the underlying cis- and trans-regulatory differences suggests that compensatory changes accumulate primarily due to selection against divergence in gene expression as a result of weak stabilizing selection on gene expression levels. These results show that cis-regulatory differences and compensatory changes in regulation play increasingly important roles in the evolution of gene expression as time increases.

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Deciphering the genic basis of environmental adaptations by simultaneous forward and reverse genetics inSaccharomyces cerevisiae

Cited by 3 publications

References 72 publications

Testing the neutral hypothesis of phenotypic evolution

Testing the neutral hypothesis of phenotypic evolution

Intra- and inter-specific variations of gene expression levels in yeast are largely neutral

Evolutionary Dynamics of Regulatory Changes Underlying Gene Expression Divergence among Saccharomyces Species

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