scholarly journals Gene regulatory evolution in cold-adapted fly populations neutralizes plasticity and may undermine genetic canalization

2022 ◽  
Author(s):  
Yuheng Huang ◽  
Justin Lack ◽  
Grant Hoppel ◽  
John E Pool
Keyword(s):  
Gene Expression ◽  
Alternative Splicing ◽  
Adaptive Evolution ◽  
Empirical Studies ◽  
Natural Populations ◽  
Plastic Response ◽  
Cold Adapted ◽  
Thermal Environments ◽  
Gene Regulatory ◽  
Transcriptomic Level

The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here we take advantage of three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution.

scholarly journals Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Genetics ◽  
2021 ◽  
Author(s):  
Yuheng Huang ◽  
Justin B Lack ◽  
Grant T Hoppel ◽  
John E Pool
Keyword(s):  
Adaptive Evolution ◽  
Parallel Evolution ◽  
Natural Populations ◽  
Population Variation ◽  
Specific Gene ◽  
Regulatory Evolution ◽  
Cold Adapted ◽  
Thermal Environments ◽  
Gene Regulatory ◽  
Trans Regulation

Abstract Changes in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find evidence for parallel expression evolution between them, with stronger parallelism at larval and adult stages than for pupae. We also implement a flexible method to estimate cis- versus trans-encoded contributions to expression or splicing differences at the adult stage. The apparent contributions of cis- versus trans-regulation to adaptive evolution vary substantially among population pairs. While two of three population pairs show a greater enrichment of cis-regulatory differences among adaptation candidates, trans-regulatory differences are more likely to be implicated in parallel expression changes between population pairs. Genes with significant cis-effects are enriched for signals of elevated genetic differentiation between cold- and warm-adapted populations, suggesting that they are potential targets of local adaptation. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.

scholarly journals Evolution of Gene Expression and Splicing in Parallel Cold-Adapted Fly Populations

2019 ◽  
Author(s):  
Yuheng Huang ◽  
Justin B. Lack ◽  
Grant T. Hoppel ◽  
John E. Pool
Keyword(s):  
Gene Expression ◽  
Adaptive Evolution ◽  
Parallel Evolution ◽  
Population Variation ◽  
Regulatory Evolution ◽  
Cold Adapted ◽  
Mitochondrial Functions ◽  
Expression Evolution ◽  
Gene Regulatory ◽  
Trans Regulation

AbstractChanges in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find significant although somewhat limited evidence for parallel expression evolution between them, and less evidence for parallel splicing evolution. We find that genes with mitochondrial functions are particularly enriched among candidates for adaptive expression evolution. We also develop a method to estimate cis-versus trans-encoded contributions to expression or splicing differences that does not rely on the presence of fixed differences between parental strains. Applying this method, we infer important roles of both cis-and trans-regulation among our putatively adaptive expression and splicing differences. The apparent contributions of cis-versus trans-regulation to adaptive evolution vary substantially among population pairs, with an Ethiopian pair showing pervasive trans-effects, suggesting that basic characteristics of regulatory evolution may depend on biological context. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.

scholarly journals The importance of alternative splicing in adaptive evolution

2021 ◽  
Author(s):  
Pooja Singh ◽  
Ehsan Pashay Ahi
Keyword(s):  
Gene Expression ◽  
Alternative Splicing ◽  
Adaptive Evolution ◽  
Adaptive Divergence ◽  
Mrna Isoforms ◽  
Evolutionary Transitions ◽  
Splice Variation ◽  
Gene Regulatory ◽  
Splice Forms

Although alternative splicing is a ubiquitous gene regulatory mechanism in plants and animals, its contribution to evolutionary transitions is understudied. Splicing enables different mRNA isoforms to be generated from the same gene, expanding transcriptomic and proteomic diversity. While the role of gene expression 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 splicing in adaptive evolution. We discuss the contribution of standing splice variation to phenotypic plasticity and how hybridisation can produce novel splice forms. Going forwards, we propose that splicing be included as a standard analysis alongside gene expression analysis so we can better understand of how splicing contributes to adaptive divergence at the micro- and macroevolutionary levels.

scholarly journals Decreased Temperature Sensitivity of Vestigial Gene Expression in Temperate Populations of Drosophila melanogaster

Genes ◽  
2019 ◽  
Vol 10 (7) ◽  
pp. 498
Author(s):  
Voigt ◽  
Erpf ◽  
Stephan
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Temperature Sensitivity ◽  
Natural Populations ◽  
Limiting Factor ◽  
Temperature Sensitive ◽  
Thermal Environments ◽  
Wide Range ◽  
Key Factor ◽  
Temperate Climates

Drosophila melanogaster recently spread from its tropical origin in Africa and became a cosmopolitan species that has adapted to a wide range of different thermal environments, including temperate climates. An important limiting factor of temperate climates has probably been their low and varying temperatures. The transcriptional output of genes can vary across temperatures, which might have been detrimental while settling in temperate environments. The reduction of temperature-sensitive expression of functionally important genes to ensure consistent levels of gene expression might have been relevant while adapting to such environments. In this study, we focus on the gene vestigial (vg) whose product is a key factor in wing development. We provide evidence that temperature-sensitivity of vg has been buffered in populations from temperate climates. We investigated temperature-sensitivity of vg gene expression in six natural populations, including four temperate populations (three from Europe and one from high-altitude Africa), and two tropical populations from the ancestral species range. All temperate populations exhibited a lower degree of temperature-induced expression plasticity than the tropical populations.

scholarly journals The Evolution of Phenotypic Plasticity in Response to Temperature Stress

2020 ◽  
Vol 12 (12) ◽  
pp. 2429-2440
Author(s):  
Francois Mallard ◽  
Viola Nolte ◽  
Christian Schlötterer
Keyword(s):  
Gene Expression ◽  
Phenotypic Plasticity ◽  
Extreme Environments ◽  
Natural Populations ◽  
Ancestral Population ◽  
Thermal Environments ◽  
Cold Environments ◽  
Thermal Plasticity ◽  
Different Temperatures ◽  
Response To Temperature

Abstract Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to environmental variation. The importance of phenotypic plasticity in natural populations and its contribution to phenotypic evolution during rapid environmental change is widely debated. Here, we show that thermal plasticity of gene expression in natural populations is a key component of its adaptation: evolution to novel thermal environments increases ancestral plasticity rather than mean genetic expression. We determined the evolution of plasticity in gene expression by conducting laboratory natural selection on a Drosophila simulans population in hot and cold environments. After more than 60 generations in the hot environment, 325 genes evolved a change in plasticity relative to the natural ancestral population. Plasticity increased in 75% of these genes, which were strongly enriched for several well-defined functional categories (e.g., chitin metabolism, glycolysis, and oxidative phosphorylation). Furthermore, we show that plasticity in gene expression of populations exposed to different temperatures is rather similar across species. We conclude that most of the ancestral plasticity can evolve further in more extreme environments.

scholarly journals Single-Cell Analysis of Alternative Splicing and Gene Regulatory Network Reveals Remarkable Expression and Regulation Dynamics During Early Embryonic Development

2021 ◽  
Author(s):  
Jiwei Chen ◽  
Yunjin Li ◽  
Geng Chen ◽  
Tieliu Shi
Keyword(s):  
Gene Expression ◽  
Alternative Splicing ◽  
Embryonic Development ◽  
Regulatory Network ◽  
Regulatory Networks ◽  
Early Embryonic Development ◽  
Expression Level ◽  
Specific Gene ◽  
Isoform Switching ◽  
Gene Regulatory

Abstract BackgroundSingle-cell RNA-seq (scRNA-seq) technologies greatly revolutionized our understanding of cell-to-cell variability of gene expression. Although several studies investigated the expression profile of early embryos, they mainly focused on the expression changes at gene level. Here we systematically explored the gene expression dynamics of human early embryonic development from expression level, alternative splicing, isoform switching and expression regulatory network. ResultsWe found that the genes involved in significant changes of these three aspects are all gradually decreased along embryonic development from E3 to E7 stage. Moreover, these three types of variations are complementary for profiling expression dynamics and they vary greatly across embryonic development as well as between different sexes. Strikingly, only a small number of genes exhibited prominent expression level changes between male and female embryos in E3 stage, whereas many more genes showed variations in alternative splicing and major isoform switching. Additionally, we identified functionally important specific gene regulatory modules for each stage and revealed dynamic usage of transcription factor binding motifs (TFBMs). ConclusionsCollectively, our study gain insights into the expression dynamics of early embryonic development from expression level, alternative splicing, isoform switching and gene regulatory networks, which could benefit the understanding of underlying mechanism of embryonic development.

scholarly journals Sex in the wild: how and why field-based studies contribute to solving the problem of sex

2017 ◽  
Author(s):  
Maurine Neiman ◽  
Patrick G. Meirmans ◽  
Tanja Schwander ◽  
Stephanie Meirmans
Keyword(s):  
Adaptive Evolution ◽  
Evolutionary Biology ◽  
Empirical Studies ◽  
Empirical Evaluation ◽  
Natural Populations ◽  
Strong Support ◽  
Niche Differentiation ◽  
In The Wild ◽  
Supplementary Material

AbstractWhy and how sexual reproduction is maintained in natural populations, the so-called “queen of problems”, is a key unanswered question in evolutionary biology. Recent efforts to solve the problem of sex have often emphasized results generated from laboratory settings. Here, we use a survey of representative “sex in the wild” literature to review and synthesize the outcomes of empirical studies focused on natural populations. Especially notable results included relatively strong support for mechanisms involving niche differentiation and a near absence of attention to adaptive evolution. Support for a major role of parasites is largely confined to a single study system, and only three systems contribute most of the support for mutation accumulation hypotheses. This evidence for taxon specificity suggests that outcomes of particular studies should not be more broadly extrapolated without extreme caution. We conclude by suggesting steps forward, highlighting tests of niche differentiation mechanisms in both lab and nature and empirical evaluation of adaptive evolution-focused hypotheses in the wild. We also emphasize the value of leveraging the growing body of genomic resources for non-model taxa to address whether the clearance of harmful mutations and spread of beneficial variants in natural populations proceeds as expected under various hypotheses for sex.Author contributionsSM and MN conceived the paper idea, SM, PM, MN, and TS designed the review strategy, reviewed and analysed the literature, and wrote the manuscript. All authors gave final approval for publication.Data archival locationThe results of our literature survey are provided as electronic supplementary material.

scholarly journals Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

2020 ◽  
Author(s):  
Arne Jacobs ◽  
Kathryn R. Elmer
Keyword(s):  
Gene Expression ◽  
Alternative Splicing ◽  
Differential Gene Expression ◽  
Differentially Expressed Genes ◽  
Adaptive Evolution ◽  
Salmonid Fish ◽  
Differentially Expressed ◽  
Molecular Processes ◽  
Regulatory Regions ◽  
Differential Gene

AbstractUnderstanding the contribution of different molecular processes to the evolution and development of divergent phenotypes is crucial for identifying the molecular routes of rapid adaptation. Here, we used RNA-seq data to compare patterns of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into benthic and pelagic ecotypes across multiple independent lakes.We found that genes that were differentially spliced and differentially expressed between the benthic and pelagic ecotypes were mostly independent (<6% overlap) and were involved in different processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were mostly involved in energy metabolism, immunity and growth. Together, these likely explain different axes of divergence between ecotypes in swimming performance and activity. Furthermore, we found that alternative splicing and gene expression are mostly controlled by independent cis-regulatory quantitative trait loci (<3.4% overlap). Cis-regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7 - 10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks (‘hub genes’) and were annotated to significantly more gene ontology terms compared to non-differentially spliced genes, consistent with a higher level of connectivity and pleiotropy.Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary phenotypes important for local adaptation. This study provides novel insights into the importance of contrasting but putatively complementary molecular processes for rapid and parallel adaptive evolution.

scholarly journals Variation in gene expression patterns across a conifer hybrid zone highlights the architecture of adaptive evolution under novel selective pressures

2021 ◽  
Author(s):  
Mitra Menon ◽  
Jared Swenson ◽  
Ehren Moler ◽  
Amy V Whipple ◽  
Kristen M Waring ◽  
...  
Keyword(s):  
Gene Expression ◽  
Adaptive Evolution ◽  
Hybrid Zone ◽  
Expression Patterns ◽  
Natural Populations ◽  
Forest Tree ◽  
Climatic Conditions ◽  
Adaptive Potential ◽  
Selective Pressures ◽  
Time Substitution

Variation in gene expression among natural populations are key contributors to adaptive evolution. Understanding the architecture underlying adaptive trait evolution provides insights into the adaptive potential of populations exposed to novel selective pressures. We investigated patterns and processes driving trait differentiation under novel climatic conditions by combining common garden experiments with transcriptome-wide datasets obtained from Pinus strobiformis - Pinus flexilis hybrid zone populations. We found strong signals of genotype-environment interactions at the individual transcript and the co-expression module level, a marked influence of drought related variables on adaptive evolution and an environment dependent influence of P. flexilis ancestry on survival. Using co-expression network connectivity as a proxy for pleiotropy we highlight that adaptive transcripts were pleiotropic across both gardens and modules with strong population differentiation exhibited lower preservation across gardens. Our work highlights the utility of integrating transcriptomics with space-for-time substitution studies to evaluate the adaptive potential of long-lived species. We conclude by suggesting that the combination of pleiotropic trait architectures and substantial genetic variation may enable long-lived forest tree species to respond to rapid shift in climatic conditions.

scholarly journals The evolution of phenotypic plasticity in response to temperature stress

2020 ◽  
Author(s):  
Francois Mallard ◽  
Viola Nolte ◽  
Christian Schlötterer
Keyword(s):  
Gene Expression ◽  
Phenotypic Plasticity ◽  
Extreme Environments ◽  
Natural Populations ◽  
Ancestral Population ◽  
Thermal Environments ◽  
Cold Environments ◽  
Thermal Plasticity ◽  
Different Temperatures ◽  
Response To Temperature

AbstractPhenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to environmental variation. The importance of phenotypic plasticity in natural populations and its contribution to phenotypic evolution during rapid environmental change is widely debated. Here, we show that thermal plasticity of gene expression in natural populations is a key component of its adaptation: evolution to novel thermal environments increases ancestral plasticity rather than mean genetic expression. We determined the evolution of plasticity in gene expression by conducting laboratory natural selection on a Drosophila simulans population in hot and cold environments. After more than 60 generations in the hot environment, 325 genes evolved a change in plasticity relative to the natural ancestral population. Plasticity increased in 75% of these genes, which were strongly enriched for several well-defined functional categories (e.g. chitin metabolism, glycolysis and oxidative phosphorylation). Furthermore, we show that plasticity in gene expression of populations exposed to different temperatures is rather similar across species. We conclude that most of the ancestral plasticity can evolve further in more extreme environments.

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