Temperature Stress Mediates Decanalization and Dominance of Gene Expression in Drosophila melanogaster

Chen, Jun; Nolte, Viola; Schlötterer, Christian

doi:10.1371/journal.pgen.1004883

Cited by 93 publications

(120 citation statements)

References 67 publications

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“…Thus, at the F 2 ‐generation they seemed to exhibit strong canalization which broke down at the F 5 ‐generation potentially due to selection, and gene expression remained decanalized at the F 11 ‐generation. Decanalization could uncover hidden gene expression variance (Chen, Nolte, & Schlötterer, ). If decanalization was stronger among random‐harvested fish, this could have led to increased gene expression variance compared to the large‐harvested fish.…”

Section: Discussionmentioning

confidence: 99%

Rapid, broad‐scale gene expression evolution in experimentally harvested fish populations

et al. 2017

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Gene expression changes potentially play an important role in adaptive evolution under human-induced selection pressures, but this has been challenging to demonstrate in natural populations. Fishing exhibits strong selection pressure against large body size, thus potentially inducing evolutionary changes in life history and other traits that may be slowly reversible once fishing ceases. However, there is a lack of convincing examples regarding the speed and magnitude of fisheries-induced evolution, and thus, the relevant underlying molecular-level effects remain elusive. We use wild-origin zebrafish (Danio rerio) as a model for harvest-induced evolution. We experimentally demonstrate broad-scale gene expression changes induced by just five generations of size-selective harvesting, and limited genetic convergence following the cessation of harvesting. We also demonstrate significant allele frequency changes in genes that were differentially expressed after five generations of size-selective harvesting. We further show that nine generations of captive breeding induced substantial gene expression changes in control stocks likely due to inadvertent selection in the captive environment. The large extent and rapid pace of the gene expression changes caused by both harvest-induced selection and captive breeding emphasizes the need for evolutionary enlightened management towards sustainable fisheries.

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Section: Discussionmentioning

confidence: 99%

Rapid, broad‐scale gene expression evolution in experimentally harvested fish populations

et al. 2017

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“…This seems to be a reasonable assumption for our experiment, given that the lines were maintained at low to moderate densities (approximately 20–100 individuals/vial/generation) and a temperature (18°C) that should be nonstressful for cosmopolitan D. melanogaster (Chen et al. ). Under these conditions, selection should be relatively ineffective and drift should dominate within lines.…”

Section: Methodsmentioning

confidence: 97%

Parallel trait adaptation across opposing thermal environments in experimentalDrosophila melanogasterpopulations

2015

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Thermal stress is a pervasive selective agent in natural populations that impacts organismal growth, survival, and reproduction. Drosophila melanogaster exhibits a variety of putatively adaptive phenotypic responses to thermal stress in natural and experimental settings; however, accompanying assessments of fitness are typically lacking. Here, we quantify changes in fitness and known thermal tolerance traits in replicated experimental D. melanogaster populations following more than 40 generations of evolution to either cyclic cold or hot temperatures. By evaluating fitness for both evolved populations alongside a reconstituted starting population, we show that the evolved populations were the best adapted within their respective thermal environments. More strikingly, the evolved populations exhibited increased fitness in both environments and improved resistance to both acute heat and cold stress. This unexpected parallel response appeared to be an adaptation to the rapid temperature changes that drove the cycling thermal regimes, as parallel fitness changes were not observed when tested in a constant thermal environment. Our results add to a small, but growing group of studies that demonstrate the importance of fluctuating temperature changes for thermal adaptation and highlight the need for additional work in this area.

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“…Heritable variation in gene expression results from genetic variation affecting cis-regulatory elements (e.g., promoters and enhancers) and trans-acting factors (e.g., proteins and RNAs). These trans-regulatory changes are located throughout the genome and are the major source of regulatory variation within species (Wittkopp et al 2004;Wang et al 2007;Sung et al 2009;Zhang and Borevitz 2009;Emerson et al 2010;Bell et al 2013;Schaefke et al 2013;Suvorov et al 2013;Coolon et al 2014;Chen et al 2015). The number, identity, and effects of individual loci contributing to variation in gene expression have been determined in a variety of species using expression quantitative trait locus (eQTL) mapping (Gilad et al 2008;Hansen et al 2008;Majewski and Pastinen 2011;Cubillos et al 2012;Nica and Dermitzakis 2013;Westra and Franke 2014;Albert and Kruglyak 2015;Pai et al 2015), with the most extensive dissection of eQTL coming from studies of two strains of the baker's yeast Saccharomyces cerevisiae (Brem et al 2002Schadt et al 2003;Yvert et al 2003;Ronald et al 2005;Smith and Kruglyak 2008;Albert et al 2014Albert et al , 2018Parts et al 2014).…”

Section: Impact Summarymentioning

confidence: 99%

“…; Chen et al. ). The number, identity, and effects of individual loci contributing to variation in gene expression have been determined in a variety of species using expression quantitative trait locus (eQTL) mapping (Gilad et al.…”

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confidence: 99%

Compensatorytrans-regulatory alleles minimizing variation inTDH3expression are common withinSaccharomyces cerevisiae

Metzger

Wittkopp

2019

Evolution Letters

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Heritable variation in gene expression is common within species. Much of this variation is due to genetic differences outside of the gene with altered expression and is trans‐acting. This trans‐regulatory variation is often polygenic, with individual variants typically having small effects, making the genetic architecture and evolution of trans‐regulatory variation challenging to study. Consequently, key questions about trans‐regulatory variation remain, including the variability of trans‐regulatory variation within a species, how selection affects trans‐regulatory variation, and how trans‐regulatory variants are distributed throughout the genome and within a species. To address these questions, we isolated and measured trans‐regulatory differences affecting TDH3 promoter activity among 56 strains of Saccharomyces cerevisiae, finding that trans‐regulatory backgrounds varied approximately twofold in their effects on TDH3 promoter activity. Comparing this variation to neutral models of trans‐regulatory evolution based on empirical measures of mutational effects revealed that despite this variability in the effects of trans‐regulatory backgrounds, stabilizing selection has constrained trans‐regulatory differences within this species. Using a powerful quantitative trait locus mapping method, we identified ∼100 trans‐acting expression quantitative trait locus in each of three crosses to a common reference strain, indicating that regulatory variation is more polygenic than previous studies have suggested. Loci altering expression were located throughout the genome, and many loci were strain specific. This distribution and prevalence of alleles is consistent with recent theories about the genetic architecture of complex traits. In all mapping experiments, the nonreference strain alleles increased and decreased TDH3 promoter activity with similar frequencies, suggesting that stabilizing selection maintained many trans‐acting variants with opposing effects. This variation may provide the raw material for compensatory evolution and larger scale regulatory rewiring observed in developmental systems drift among species.

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Temperature Stress Mediates Decanalization and Dominance of Gene Expression in Drosophila melanogaster

Cited by 93 publications

References 67 publications

Rapid, broad‐scale gene expression evolution in experimentally harvested fish populations

Rapid, broad‐scale gene expression evolution in experimentally harvested fish populations

Parallel trait adaptation across opposing thermal environments in experimentalDrosophila melanogasterpopulations

Compensatorytrans-regulatory alleles minimizing variation inTDH3expression are common withinSaccharomyces cerevisiae

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