Variation within and among species in gene expression: raw material for evolution

Whitehead, Andrew; Crawford, Douglas L.

doi:10.1111/j.1365-294x.2006.02868.x

Cited by 335 publications

(319 citation statements)

References 100 publications

(254 reference statements)

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“…Instead, we find that expression divergence between orthologous genes saturates rapidly in evolutionary time. This general pattern was previously hypothesized to exist by Whitehead and Crawford (20). Species pairs of Drosophila do not show a significant increase in expression divergence beyond that present between D. melanogaster and D. ananasse.…”

Section: Resultsmentioning

confidence: 64%

Optimization of gene expression by natural selection

Bedford

Hartl

2009

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

186

229

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It is generally assumed that stabilizing selection promoting a phenotypic optimum acts to shape variation in quantitative traits across individuals and species. Although gene expression represents an intensively studied molecular phenotype, the extent to which stabilizing selection limits divergence in gene expression remains contentious. In this study, we present a theoretical framework for the study of stabilizing and directional selection using data from between-species divergence of continuous traits. This framework, based upon Brownian motion, is analytically tractable and can be used in maximum-likelihood or Bayesian parameter estimation. We apply this model to gene-expression levels in 7 species of Drosophila, and find that gene-expression divergence is substantially curtailed by stabilizing selection. However, we estimate the selective effect, s, of gene-expression change to be very small, approximately equal to Ns for a change of one standard deviation, where N is the effective population size. These findings highlight the power of natural selection to shape phenotype, even when the fitness effects of mutations are in the nearly neutral range.evolution ͉ nearly neutral ͉ Ornstein-Uhlenbeck ͉ phenotypic optima A bundant evidence indicates that natural selection is remarkably powerful in shaping nucleotide sequences (1, 2). Many tests of natural selection rely on a comparison between nonsynonymous sites, in which mutations affect protein sequence, and synonymous sites, in which mutations do not. Synonymous sites serve as a proxy for neutral sites, enabling the effects of selection to be distinguished from background mutational and demographic patterns. Although changes in gene expression are hypothesized to play a major role in adaptation (3, 4), changes in expression cannot be so easily partitioned into neutral and selected categories. Thus, methods derived to analyze selection in coding sequences cannot be readily applied to gene-expression data. In part because of this ambiguity, general forces acting on gene-expression divergence have remained unclear. At this point, there exists considerable debate over the relative importance of selection and random drift in shaping gene-expression levels (5-8).The benefits of optimal gene regulation seem in many ways obvious. In the simple case of metabolic enzymes, underexpression may slow metabolic flux, while over-expression may expose the cell to additional toxic misfolded proteins (9). At the morphological level, gene regulation can be tightly coupled to phenotype (10, 11). Genetic mutations whose effects cascade into morphological differences are expected to have especially large fitness impacts, and as such will be heavily influenced by natural selection. A straightforward example of selection on gene-expression level can be seen in ribosomal proteins, which contrary to the neutral prediction are found to be highly expressed across a variety of organisms (12).In this article, we present a model of gene-expression divergence that explicitly distinguishes betw...

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Section: Resultsmentioning

confidence: 64%

Optimization of gene expression by natural selection

Bedford

Hartl

2009

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

186

229

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“…Therefore, it is not surprising that RNA-seq has become the technology of choice for quantifying differential gene expression (Deng et al, 2011;Smith et al, 2013). Gene expression analyses have allowed the identification of key molecular mechanisms underlying desired traits in farmed fish (Roberge et al, 2006;Ferraresso et al, 2008Ferraresso et al, , 2013, but have also been successfully applied to natural populations of marine fishes (Whitehead and Crawford, 2006;Larsen et al, 2007Larsen et al, , 2011Pujolar et al, 2012Pujolar et al, , 2013bCôté et al, 2014). Finally, transcriptomic analyses can be complemented and integrated with protein expression analysis to investigate the responses at the proteomic level for a deeper understanding of functional implications (Nie et al, 2007;Dalziel and Schulte, 2012).…”

Section: Linking Genotype and Phenotypementioning

confidence: 99%

Population Genomics of Marine Fishes: Next-Generation Prospects and Challenges

Hemmer‐Hansen

Therkildsen

Pujolar

2014

The Biological Bulletin

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“…Numerous studies have characterized genomewide patterns of gene expression among populations exhibiting phenotypic variation. In fishes in particular, the majority of such studies have not only used microarrays (Oleksiak et al, 2002;Whitehead and Crawford, 2005;Whitehead and Crawford, 2006;St-Cyr et al, 2008;Whiteley et al, 2008), but also next-generation sequencing to a lower extent (Elmer et al, 2010;Goetz et al, 2010;Jeukens et al, 2010;Shen et al, 2012). Hybridization can also lead to different modes of transcription regulation.…”

Section: Introductionmentioning

confidence: 99%

Linking transcriptomic and genomic variation to growth in brook charr hybrids (Salvelinus fontinalis, Mitchill)

Bougas¹,

Normandeau²,

Audet³

et al. 2013

Heredity

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Hybridization can lead to phenotypic differences arising from changes in gene expression patterns or new allele combinations. Variation in gene expression is thought to be controlled by differences in transcription regulation of parental alleles, either through cis-or trans-regulatory elements. A previous study among brook charr hybrids from different populations (Rupert, Laval, and domestic) showing distinct length at age during early life stages also revealed different patterns in transcription regulation inheritance of transcript abundance. In the present study, transcript abundance using RNA-sequencing and quantitative real-time PCR, single-nucleotide polymorphism (SNP) genotypes and allelic imbalance were assessed in order to understand the molecular mechanisms underlying the observed transcriptomic and differences in length at age among domestic Â Rupert hybrids and Laval Â domestic hybrids. We found 198 differentially expressed genes between the two hybrid crosses, and allelic imbalance could be analyzed for 69 of them. Among these 69 genes, 36 genes exhibited cis-acting regulatory effects in both of the two crosses, thus confirming the prevalent role of cis-acting regulatory elements in the regulation of differentially expressed genes among intraspecific hybrids. In addition, we detected a significant association between SNP genotypes of three genes and length at age. Our study is thus one of the few that have highlighted some of the molecular mechanisms potentially involved in the differential phenotypic expression in intraspecific hybrids for nonmodel species.

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Variation within and among species in gene expression: raw material for evolution

Cited by 335 publications

References 100 publications

Optimization of gene expression by natural selection

Optimization of gene expression by natural selection

Population Genomics of Marine Fishes: Next-Generation Prospects and Challenges

Linking transcriptomic and genomic variation to growth in brook charr hybrids (Salvelinus fontinalis, Mitchill)

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