Gene expression links genotype and phenotype during rapid adaptation

Josephs, Emily B.

doi:10.1111/mec.15729

Cited by 10 publications

(8 citation statements)

References 11 publications

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“…Unlike changes in coding genes, changes in gene expression can speed up adaptive evolution, especially under strong selection pressures over short timescales (Brauer et al, 2017; Jones et al, 2012; Uusi-Heikkilä et al, 2017). More explicitly, changes in gene expression are expected to respond quicker than mutations in coding sequences when a population colonises a novel environment (Josephs, 2021). In fact, only gene expression effects can be moulded to enhance or inhibit the role of genes in a particular tissue(s).…”

Section: Discussionmentioning

confidence: 99%

Gene expression shifts in Emperor penguin adaptation to the extreme Antarctic environment

Paris,

Fernandes,

Pirri

et al. 2023

Preprint

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Gene expression can accelerate ecological divergence by rapidly tweaking the response of an organism to novel environments, with more divergent environments exerting stronger selection and, supposedly, requiring faster adaptive responses. Organisms adapted to extreme environments provide ideal systems to test this hypothesis, particularly when compared to related species with milder ecological niches. The Emperor penguin (Aptenodytes forsteri) is the only warm-blooded vertebrate breeding in the harsh Antarctic winter, in stark contrast with the less cold-adapted sister species, the King penguin (A. patagonicus). Assembling the firstde novotranscriptomes and analysing multi-tissue (brain, kidney, liver, muscle, skin) RNAseq data from natural populations of both species, we quantified the shifts in tissue-enhanced genes, co-expression gene networks, and differentially expressed genes characterising Emperor penguin adaptation to extreme Antarctic ecology. Our analyses revealed the crucial role played by muscle and liver in temperature homeostasis, fasting and whole-body energy metabolism (glucose/insulin regulation, lipid metabolism, fatty acid beta-oxidation, and blood coagulation). Repatterning at the regulatory level appears as more important in the brain of the Emperor penguin, showing the lowest signature of differential gene expression but the largest co-expression gene network shift. Nevertheless, over-expressed genes related to mTOR signalling in the brain and the liver support their central role in cold and fasting responses. Besides contributing to understanding the genetics underlying complex traits, like body energy reservoir management, our results provide a first insight into the role of gene expression in adaptation to one of the most extreme environmental conditions endured by an endotherm.

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Section: Discussionmentioning

confidence: 99%

Gene expression shifts in Emperor penguin adaptation to the extreme Antarctic environment

Paris,

Fernandes,

Pirri

et al. 2023

Preprint

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“…Both variation in gene expression and alternative splicing have the potential to impact phenotypic variation (Gueroussov et al, 2015;Josephs, 2021) (Figure 2). While gene promoter activity quantitatively regulates the number of transcripts, alternative splicing changes the structure of transcripts and the encoded proteins (Tellier, Maudlin, & Murphy, 2020).…”

Section: Alternative Splicing As a Substrate For Adaptive Evolution At Long And Short Timescalesmentioning

confidence: 99%

The importance of alternative splicing in adaptive evolution

Singh

Ahi

2022

Molecular Ecology

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Although alternative splicing is a ubiquitous gene regulatory mechanism in plants, animals and fungi, its contribution to evolutionary transitions is understudied. Alternative splicing enables different mRNA isoforms to be generated from the same gene, expanding transcriptomic and thus proteomic diversity. While the role of gene expression variation in adaptive evolution is widely accepted, biologists still debate the functional impact of alternative isoforms on phenotype. In light of recent empirical research linking splice variation to ecological adaptations, we propose that alternative splicing is an important substrate for adaptive evolution and speciation, particularly at short timescales. We synthesise what is known about the role of alternative splicing in adaptive evolution. We discuss the contribution of standing splice variation to phenotypic plasticity and how hybridisation can produce novel Opinion 2 splice forms. Going forwards, we propose that alternative splicing be included as a standard analysis alongside gene expression analysis so we can better understand of how alternative splicing contributes to adaptive divergence at the micro-and macroevolutionary levels.

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“…Gene expression is among the most well-known molecular plastic traits, mainly because transcriptional regulations, which link genotypes and phenotypes, can be immediately induced to cope with environmental stresses during many ecological and evolutionary processes ( Fu et al 2021 ; Josephs 2021 ). Many studies have examined the roles of gene expression plasticity in organismal acclimation and adaptation to various environmental changes.…”

Section: Introductionmentioning

confidence: 99%

Multidimensional plasticity jointly contributes to rapid acclimation to environmental challenges during biological invasions

Huang

Shenkar

et al. 2023

RNA

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Rapid plastic response to environmental changes, which involves extremely complex underlying mechanisms, is crucial for organismal survival during many ecological and evolutionary processes such as those in global change and biological invasions. Gene expression is among the most studied molecular plasticity, while co- or post-transcriptional mechanisms are still largely unexplored. Using a model invasive ascidian Ciona savignyi, we studied multidimensional short-term plasticity in response to hyper- and hypo-salinity stresses, covering the physiological adjustment, gene expression, alternative splicing (AS), and alternative polyadenylation (APA) regulations. Our results demonstrated that rapid plastic response varied with environmental context, timescales, and molecular regulatory levels. Gene expression, AS, and APA regulations independently acted on different gene sets and corresponding biological functions, highlighting their non-redundant roles in rapid environmental adaptation. Stress-induced gene expression changes illustrated the use of a strategy of accumulating free amino acid under high salinity and losing/reducing them during low salinity to maintain the osmotic homoeostasis. Genes with more exons were inclined to use AS regulations, and isoform switches in functional genes such as SLC2a5 and Cyb5r3 resulted in enhanced transporting activities by upregulating the isoforms with more transmembrane regions. The extensive 3'-untranslated region (3'UTR) shortening through APA was induced by both salinity stresses, and APA regulation predominated transcriptomic changes at some stages of stress response. The findings here provide evidence for complex plastic mechanisms to environmental changes, and thereby highlight the importance of systemically integrating different levels of regulatory mechanisms in studying initial plasticity in evolutionary trajectories.

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Gene expression links genotype and phenotype during rapid adaptation

Cited by 10 publications

References 11 publications

Gene expression shifts in Emperor penguin adaptation to the extreme Antarctic environment

Gene expression shifts in Emperor penguin adaptation to the extreme Antarctic environment

The importance of alternative splicing in adaptive evolution

Multidimensional plasticity jointly contributes to rapid acclimation to environmental challenges during biological invasions

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