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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. 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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3. 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)

   Abstract 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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4. Plasticity-mediated persistence and subsequent local adaptation in a global agricultural weed

   https://doi.org/10.1093/evolut/qpae109  

   Garrison, Ava_J; Norwood, Lauren_A; Conner, Jeffrey_K; Spigler, ed., Rachel; Wolf, ed., Jason (July 2024, Evolution)

   Abstract Phenotypic plasticity can alter traits that are crucial to population establishment in a new environment before adaptation can occur. How often phenotypic plasticity enables subsequent adaptive evolution is unknown, and examples of the phenomenon are limited. We investigated the hypothesis of plasticity-mediated persistence as a means of colonization of agricultural fields in one of the world’s worst weeds, Raphanus raphanistrum ssp. raphanistrum. Using non-weedy native populations of the same species and subspecies as a comparison, we tested for plasticity-mediated persistence in a growth chamber reciprocal transplant experiment. We identified traits with genetic differentiation between the weedy and native ecotypes as well as phenotypic plasticity between growth chamber environments. We found that most traits were both plastic and differentiated between ecotypes, with the majority plastic and differentiated in the same direction. This suggests that phenotypic plasticity may have enabled radish populations to colonize and then adapt to novel agricultural environments. 

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5. Gene expression and alternative splicing contribute to adaptive divergence of ecotypes

   https://doi.org/10.1038/s41437-023-00665-y  

   Innes, Peter A; Goebl, April M; Smith, Chris_C R; Rosenberger, Kaylee; Kane, Nolan C (March 2024, Heredity)

   Regulation of gene expression is a critical link between genotype and phenotype explaining substantial heritable variation within species. However, we are only beginning to understand the ways that specific gene regulatory mechanisms contribute to adaptive divergence of populations. In plants, the post-transcriptional regulatory mechanism of alternative splicing (AS) plays an important role in both development and abiotic stress response, making it a compelling potential target of natural selection. AS allows organisms to generate multiple different transcripts/proteins from a single gene and thus may provide a source of evolutionary novelty. Here, we examine whether variation in alternative splicing and gene expression levels might contribute to adaptation and incipient speciation of dune-adapted prairie sunflowers in Great Sand Dunes National Park, Colorado, USA. We conducted a common garden experiment to assess transcriptomic variation among ecotypes and analyzed differential expression, differential splicing, and gene coexpression. We show that individual genes are strongly differentiated for both transcript level and alternative isoform proportions, even when grown in a common environment, and that gene coexpression networks are disrupted between ecotypes. Furthermore, we examined how genome-wide patterns of sequence divergence correspond to divergence in transcript levels and isoform proportions and find evidence for both cis and trans-regulation. Together, our results emphasize that alternative splicing has been an underappreciated mechanism providing source material for natural selection at short evolutionary time scales. 

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