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1. Gene Regulatory Evolution in Cold-Adapted Fly Populations Neutralizes Plasticity and May Undermine Genetic Canalization

   https://doi.org/10.1093/gbe/evac050  

   Huang, Yuheng; Lack, Justin B.; Hoppel, Grant T.; Pool, John E. (April 2022, Genome Biology and Evolution)

   Zhang, George (Ed.)

   Abstract 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. 

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2. 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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3. Mechanisms of regulatory evolution in yeast

   https://doi.org/10.1016/j.gde.2022.101998  

   Siddiq, Mohammad A; Wittkopp, Patricia J (December 2022, Current Opinion in Genetics & Development)

   Studies of regulatory variation in yeast -- at the level of new mutations, polymorphisms within a species, and divergence between species -- have provided great insight into the molecular and evolutionary processes responsible for the evolution of gene expression in eukaryotes. The increasing ease with which yeast genomes can be manipulated and expression quantified in a high-throughput manner has recently accelerated mechanistic studies of cis- and trans-regulatory variation at multiple evolutionary timescales. These studies have, for example, identified differences in the properties of cis- and trans-acting mutations that affect their evolutionary fate, experimentally characterized the molecular mechanisms through which cis- and trans-regulatory variants act, and illustrated how regulatory networks can diverge between species with or without changes in gene expression. 

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4. The genetic regulatory architecture and epigenomic basis for age-related changes in rattlesnake venom

   https://doi.org/10.1073/pnas.2313440121  

   Hogan, Michael_P; Holding, Matthew_L; Nystrom, Gunnar_S; Colston, Timothy_J; Bartlett, Daniel_A; Mason, Andrew_J; Ellsworth, Schyler_A; Rautsaw, Rhett_M; Lawrence, Kylie_C; Strickland, Jason_L; et al (April 2024, Proceedings of the National Academy of Sciences)

   Developmental phenotypic changes can evolve under selection imposed by age- and size-related ecological differences. Many of these changes occur through programmed alterations to gene expression patterns, but the molecular mechanisms and gene-regulatory networks underlying these adaptive changes remain poorly understood. Many venomous snakes, including the eastern diamondback rattlesnake (Crotalus adamanteus), undergo correlated changes in diet and venom expression as snakes grow larger with age, providing models for identifying mechanisms of timed expression changes that underlie adaptive life history traits. By combining a highly contiguous, chromosome-level genome assembly with measures of expression, chromatin accessibility, and histone modifications, we identified cis-regulatory elements and trans-regulatory factors controlling venom ontogeny in the venom glands ofC. adamanteus. Ontogenetic expression changes were significantly correlated with epigenomic changes within genes, immediately adjacent to genes (e.g., promoters), and more distant from genes (e.g., enhancers). We identified 37 candidate transcription factors (TFs), with the vast majority being up-regulated in adults. The ontogenetic change is largely driven by an increase in the expression of TFs associated with growth signaling, transcriptional activation, and circadian rhythm/biological timing systems in adults with corresponding epigenomic changes near the differentially expressed venom genes. However, both expression activation and repression contributed to the composition of both adult and juvenile venoms, demonstrating the complexity and potential evolvability of gene regulation for this trait. Overall, given that age-based trait variation is common across the tree of life, we provide a framework for understanding gene-regulatory-network-driven life-history evolution more broadly. 

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5. Systems genomics of salinity stress response in rice

   https://doi.org/10.7554/eLife.99352.2  

   Gupta, Sonal; Groen, Simon C; Zaidem, Maricris L; Sajise, Andres_Godwin C; Calic, Irina; Natividad, Mignon A; McNally, Kenneth L; Vergara, Georgina V; Satija, Rahul; Franks, Steven J; et al (February 2025, eLIFE Science Publications)

   Populations can adapt to stressful environments through changes in gene expression. However, the fitness effect of gene expression in mediating stress response and adaptation remains largely unexplored. Here, we use an integrative field dataset obtained from 780 plants of Oryza sativa ssp. indica (rice) grown in a field experiment under normal or moderate salt stress conditions to examine selection and evolution of gene expression variation under salinity stress conditions. We find that salinity stress induces increased selective pressure on gene expression. Further, we show that trans-eQTLs rather than cis-eQTLs are primarily associated with rice’s gene expression under salinity stress, potentially via a few master-regulators. Importantly, and contrary to the expectations, we find that cis-trans reinforcement is more common than cis-trans compensation which may be reflective of rice diversification subsequent to domestication. We further identify genetic fixation as the likely mechanism underlying this compensation/reinforcement. Additionally, we show that cis- and trans-eQTLs are under balancing and purifying selection, respectively, giving us insights into the evolutionary dynamics of gene expression variation. By examining genomic, transcriptomic, and phenotypic variation across a rice population, we gain insights into the molecular and genetic landscape underlying adaptive salinity stress responses, which is relevant for other crops and other stresses. 

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