Evaluating the role of natural selection in the evolution of gene regulation

Fay, Justin C.; Wittkopp, Patricia J.

doi:10.1038/sj.hdy.6801000

Cited by 162 publications

(153 citation statements)

References 140 publications

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“…Although numerous studies of selection pressures acting on genome-wide gene expression levels have been reported (10), nearly all have found only negative selection and/or neutrality, consistent with the intuition that random changes to any functional system (including gene expression) will tend to be deleterious, and thus selected against. This is most likely because these studies were designed to detect the "average" mode of selection acting on new mutations that affect gene expression (SI Text).…”

mentioning

confidence: 88%

Evidence for widespread adaptive evolution of gene expression in budding yeast

Fraser

Moses

Schadt

2010

Proc. Natl. Acad. Sci. U.S.A.

157

183

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Changes in gene expression have been proposed to underlie many, or even most, adaptive differences between species. Despite the increasing acceptance of this view, only a handful of cases of adaptive gene expression evolution have been demonstrated. To address this discrepancy, we introduce a simple test for lineage-specific selection on gene expression. Applying the test to genome-wide gene expression data from the budding yeast Saccharomyces cerevisiae , we find that hundreds of gene expression levels have been subject to lineage-specific selection. Comparing these findings with independent population genetic evidence of selective sweeps suggests that this lineage-specific selection has resulted in recent sweeps at over a hundred genes, most of which led to increased transcript levels. Examination of the implicated genes revealed a specific biochemical pathway—ergosterol biosynthesis—where the expression of multiple genes has been subject to selection for reduced levels. In sum, these results suggest that adaptive evolution of gene expression is common in yeast, that regulatory adaptation can occur at the level of entire pathways, and that similar genome-wide scans may be possible in other species, including humans.

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mentioning

confidence: 88%

Evidence for widespread adaptive evolution of gene expression in budding yeast

Fraser

Moses

Schadt

2010

Proc. Natl. Acad. Sci. U.S.A.

157

183

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“…(a) Identifying adaptive phenotypic traits: insights from the transcriptome Ever since the pioneering work of Britten & Davidson (1971) and King & Wilson (1975) on the mechanisms and evolutionary role of regulatory processes, there has been increasing recognition that variation in levels of gene expression represents a major source of evolutionary novelty, which in turn can lead to phenotypic divergence by natural selection (Oleksiak et al 2002;Wittkopp 2007;Wray 2007;Fay & Wittkopp 2008). The development of microarray technologies, allowing the simultaneous detection of expression modulations at thousands of genes, offers a powerful means of assessing the importance of evolutionary change in gene regulation involved in adaptive population divergence (Bochdanovits et al 2003;Ranz & Machado 2005;Matzkin et al 2006).…”

Section: Identifying Adaptive Phenotypic Traitsmentioning

confidence: 99%

On the origin of species: insights from the ecological genomics of lake whitefish

Bernatchez

Renaut

Whiteley

et al. 2010

Phil. Trans. R. Soc. B

228

317

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In contrast to the large amount of ecological information supporting the role of natural selection as a main cause of population divergence and speciation, an understanding of the genomic basis underlying those processes is in its infancy. In this paper, we review the main findings of a long-term research programme that we have been conducting on the ecological genomics of sympatric forms of whitefish (Coregonus spp.) engaged in the process of speciation. We present this system as an example of how applying a combination of approaches under the conceptual framework of the theory of adaptive radiation has yielded substantial insight into evolutionary processes in a non-model species. We also discuss how the joint use of recent biotechnological developments will provide a powerful means to address issues raised by observations made to date. Namely, we present data illustrating the potential offered by combining next generation sequencing technologies with other genomic approaches to reveal the genomic bases of adaptive divergence and reproductive isolation. Given increasing access to these new genomic tools, we argue that non-model species studied in their ecological context such as whitefish will play an increasingly important role in generalizing knowledge of speciation.

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“…Recently, prospects for quantifying cis-regulatory variation have greatly improved, and, as a result, ample heritable cis-regulatory variation has been identified in many species (6); this is resulting in a growing consensus that a large amount of standing cis-regulatory variation is under weak purifying selection (7)(8)(9). Clarifying why the impact of purifying selection varies across the genome is therefore important to understand the maintenance of cis-regulatory variation.…”

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confidence: 99%

Genomic analysis reveals major determinants ofcis-regulatory variation inCapsella grandiflora

Steige

Laenen

Reimegård

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Understanding the causes of cis-regulatory variation is a long-standing aim in evolutionary biology. Although cis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standing cis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants, and selective forces shaping cis-regulatory variation in the outcrossing plant Capsella grandiflora. We first identified a set of 1,010 genes with common cis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with common cis-regulatory variation (i) are under weaker purifying selection and (ii) undergo less frequent positive selection than other genes. We further identified genomic determinants of cis-regulatory variation. Gene body methylation (gbM) was a major factor constraining cis-regulatory variation, whereas presence of nearby transposable elements (TEs) and tissue specificity of expression increased the odds of ASE. Our results suggest that most common cis-regulatory variation in C. grandiflora is under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance of cis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide evidence for a link between gbM and cis-regulatory constraint, possibly reflecting greater dosage sensitivity of body-methylated genes. Given the extensive conservation of gbM in flowering plants, this suggests that gbM could be an important predictor of cis-regulatory variation in a wide range of plant species.allele-specific expression | fitness effects | purifying selection | positive selection | gene body methylation U nderstanding the causes of regulatory variation is of major importance for many areas of biology and medicine (1). Much interest has centered on cis-regulatory variation, which has long been thought to be particularly important for adaptation (2-5). Like other quantitative traits, cis-regulatory variation is expected to be shaped by the interplay of mutation, selection, and drift. However, the relative importance of these forces remains unclear in most species.Recently, prospects for quantifying cis-regulatory variation have greatly improved, and, as a result, ample heritable cis-regulatory variation has been identified in many species (6); this is resulting in a growing consensus that a large amount of standing cis-regulatory variation is under weak purifying selection (7-9). Clarifying why the impact of purifying selection varies across the genome is therefore important to understand the maintenance of cis-regulatory variation.Variation in the intensity of purifying selection across the genome can result from differences in selective constraint that are due to the specific functions of...

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Evaluating the role of natural selection in the evolution of gene regulation

Cited by 162 publications

References 140 publications

Evidence for widespread adaptive evolution of gene expression in budding yeast

Evidence for widespread adaptive evolution of gene expression in budding yeast

On the origin of species: insights from the ecological genomics of lake whitefish

Genomic analysis reveals major determinants ofcis-regulatory variation inCapsella grandiflora

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