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1. Parallel and population-specific gene regulatory evolution in cold-adapted fly populations

   https://doi.org/10.1093/genetics/iyab077  

   Huang, Yuheng ; Lack, Justin B ; Hoppel, Grant T ; Pool, John E ( May 2021 , Genetics)

   Begun, D (Ed.)

   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- vs trans-encoded contributions to expression or splicing differences at the adult stage. The apparent contributions of cis- vs 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. 

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2. Rapid evolution of genome‐wide gene expression and plasticity during saline to freshwater invasions by the copepod Eurytemora affinis species complex

   https://doi.org/10.1111/mec.15681  

   Posavi, Marijan ; Gulisija, Davorka ; Munro, James B. ; Silva, Joana C. ; Lee, Carol Eunmi ( November 2020 , Molecular Ecology)

   Saline migrants into freshwater habitats constitute among the most destructive invaders in aquatic ecosystems throughout the globe. However, the evolutionary and physiological mechanisms underlying such habitat transitions remain poorly understood. To explore the mechanisms of freshwater adaptation and distinguish between adaptive (evolutionary) and acclimatory (plastic) responses to salinity change, we examined genome‐wide patterns of gene expression between ancestral saline and derived freshwater populations of theEurytemora affinisspecies complex, reared under two different common‐garden conditions (0 versus 15 PSU). We found that evolutionary shifts in gene expression (between saline and freshwater inbred lines) showed far greater changes and were more widespread than acclimatory responses to salinity (0 versus 15 PSU). Most notably, 30–40 genes showing evolutionary shifts in gene expression across the salinity boundary were associated with ion transport function, withinorganic cation transmembrane transportforming the largest Gene Ontology category. Of particular interest was the sodium transporter, the Na⁺/H⁺antiporter (NHA) gene family, which was discovered in animals relatively recently. Thirty key ion regulatory genes, such as NHA paralogue #7, demonstrated concordant evolutionary and plastic shifts in gene expression, suggesting the evolution of ion transporter function and plasticity during rapid invasions into novel salinities. Moreover, freshwater invasions were associated with the evolution of reduced plasticity in the freshwater population, again for the same key ion transporters, consistent with the predicted evolution of canalization following adaptation to stressful conditions. Our results have important implications for understanding evolutionary and physiological mechanisms of range expansions by some of the most widespread invaders in aquatic habitats.

    

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3. Biological invasion: The influence of the hidden side of the (epi)genome

   https://doi.org/10.1111/1365-2435.13317  

   Marin, Pierre ; Genitoni, Julien ; Barloy, Dominique ; Maury, Stéphane ; Gibert, Patricia ; Ghalambor, Cameron K. ; Vieira, Cristina ; Herrel, ed., Anthony ( March 2019 , Functional Ecology)

   Understanding the mechanisms underlying biological invasions and rapid adaptation to global change remains a fundamental challenge, particularly in small populations lacking in genetic variation. Two understudied mechanisms that could facilitate adaptive evolution and adaptive plasticity are the increased genetic variation due to transposable elements (TEs), and associated or independent modification of gene expression through epigenetic changes.

   Here, we focus on the potential role of these genetic and non‐genetic mechanisms for facilitating invasion success. Because novel or stressful environments are known to induce both epigenetic changes and TE activity, these mechanisms may play an underappreciated role in generating phenotypic and genetic variation for selection to act on. We review how these mechanisms operate, the evidence for how they respond to novel or stressful environments, and how these mechanisms can contribute to the success of biological invasions by facilitating adaptive evolution and phenotypic plasticity.

   Because genetic and phenotypic variations due to TEs and epigenetic changes are often well regulated or “hidden” in the native environment, the independent and combined contribution of these mechanisms may only become important when populations colonize novel environments. A focus on the mechanisms that generate and control the expression of this variation in new environments may provide insights into biological invasions that would otherwise not be obvious.

   Global changes and human activities impact on ecosystems and allow new opportunities for biological invasions. Invasive species succeed by adapting rapidly to new environments. The degree to which rapid responses to environmental change could be mediated by the epigenome—the regulatory system that integrates how environmental and genomic variation jointly shape phenotypic variation—requires greater attention if we want to understand the mechanisms by which populations successfully colonize and adapt to new environments.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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4. Restoring ancestral phenotypes is a general pattern in gene expression evolution during adaptation to new environments in Tribolium castaneum

   https://doi.org/10.1111/mec.15607  

   Koch, Eva L. ; Guillaume, Frédéric ( September 2020 , Molecular Ecology)

   Plasticity and evolution are two processes allowing populations to respond to environmental changes, but how both are related and impact each other remains controversial. We studied plastic and evolutionary responses in gene expression ofTribolium castaneumafter exposure of the beetles to new environments that differed from ancestral conditions in temperature, humidity or both. Using experimental evolution with 10 replicated lines per condition, we were able to demonstrate adaptation after 20 generations. We measured whole‐transcriptome gene expression with RNA‐sequencing to infer evolutionary and plastic changes. We found more evidence for changes in mean expression (shift in the intercept of reaction norms) in adapted lines than for changes in plasticity (shifts in slopes). Plasticity was mainly preserved in selected lines and was responsible for a large part of the phenotypic divergence in expression between ancestral and new conditions. However, we found that genes with the largest evolutionary changes in expression also evolved reduced plasticity and often showed expression levels closer to the ancestral stage. Results obtained in the three different conditions were similar, suggesting that restoration of ancestral expression levels during adaptation is a general evolutionary pattern. With a larger sample in the most stressful condition, we were able to detect a positive correlation between the proportion of genes with reversion of the ancestral plastic response and mean fitness per selection line.

    

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5. Adaptive Phenotypic Plasticity Stabilizes Evolution in Fluctuating Environments

   https://doi.org/10.3389/fevo.2021.715381  

   Lalejini, Alexander ; Ferguson, Austin J. ; Grant, Nkrumah A. ; Ofria, Charles ( August 2021 , Frontiers in Ecology and Evolution)

   Fluctuating environmental conditions are ubiquitous in natural systems, and populations have evolved various strategies to cope with such fluctuations. The particular mechanisms that evolve profoundly influence subsequent evolutionary dynamics. One such mechanism is phenotypic plasticity, which is the ability of a single genotype to produce alternate phenotypes in an environmentally dependent context. Here, we use digital organisms (self-replicating computer programs) to investigate how adaptive phenotypic plasticity alters evolutionary dynamics and influences evolutionary outcomes in cyclically changing environments. Specifically, we examined the evolutionary histories of both plastic populations and non-plastic populations to ask: (1) Does adaptive plasticity promote or constrain evolutionary change? (2) Are plastic populations better able to evolve and then maintain novel traits? And (3), how does adaptive plasticity affect the potential for maladaptive alleles to accumulate in evolving genomes? We find that populations with adaptive phenotypic plasticity undergo less evolutionary change than non-plastic populations, which must rely on genetic variation from de novo mutations to continuously readapt to environmental fluctuations. Indeed, the non-plastic populations undergo more frequent selective sweeps and accumulate many more genetic changes. We find that the repeated selective sweeps in non-plastic populations drive the loss of beneficial traits and accumulation of maladaptive alleles, whereas phenotypic plasticity can stabilize populations against environmental fluctuations. This stabilization allows plastic populations to more easily retain novel adaptive traits than their non-plastic counterparts. In general, the evolution of adaptive phenotypic plasticity shifted evolutionary dynamics to be more similar to that of populations evolving in a static environment than to non-plastic populations evolving in an identical fluctuating environment. All natural environments subject populations to some form of change; our findings suggest that the stabilizing effect of phenotypic plasticity plays an important role in subsequent adaptive evolution. 

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