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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 regulation and speciation in a migratory divide between songbirds

   https://doi.org/10.1038/s41467-023-44352-2  

   Louder, Matthew I. M. ; Justen, Hannah ; Kimmitt, Abigail A. ; Lawley, Koedi S. ; Turner, Leslie M. ; Dickman, J. David ; Delmore, Kira E. ( January 2024 , Nature Communications)

   Behavioral variation abounds in nature. This variation is important for adaptation and speciation, but its molecular basis remains elusive. Here, we use a hybrid zone between two subspecies of songbirds that differ in migration – an ecologically important and taxonomically widespread behavior---to gain insight into this topic. We measure gene expression in five brain regions. Differential expression between migratory states was dominated by circadian genes in all brain regions. The remaining patterns were largely brain-region specific. For example, expression differences between the subspecies that interact with migratory state likely help maintain reproductive isolation in this system and were documented in only three brain regions. Contrary to existing work on regulatory mechanisms underlying species-specific traits, two lines of evidence suggest that trans- (vs. cis) regulatory changes underlie these patterns – no evidence for allele-specific expression in hybrids and minimal associations between genomic differentiation and expression differences. Additional work with hybrids shows expression levels were often distinct (transgressive) from parental forms. Behavioral contrasts and functional enrichment analyses allowed us to connect these patterns to mitonuclear incompatibilities and compensatory responses to stress that could exacerbate selection on hybrids and contribute to speciation.

    

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3. Loss of transcriptional plasticity but sustained adaptive capacity after adaptation to global change conditions in a marine copepod

   https://doi.org/10.1038/s41467-022-28742-6  

   Brennan, Reid S. ; deMayo, James A. ; Dam, Hans G. ; Finiguerra, Michael B. ; Baumann, Hannes ; Pespeni, Melissa H. ( March 2022 , Nature Communications)

   Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod,Acartia tonsa, in future global change conditions (high temperature and high CO₂). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments.

    

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4. Parallel Evolution towards Increased Motility in Long-Term Cultures of Escherichia coli, Even Though Motility was Not Required for Long-Term Survival

   https://doi.org/10.1128/spectrum.02330-21  

   Henderson, Autumn L. ; Moreno, Angie ; Kram, Karin E. ( June 2022 , Microbiology Spectrum)

   Gao, Beile (Ed.)

   ABSTRACT Escherichia coli can survive for long periods in batch culture in the laboratory, where they experience a stressful and heterogeneous environment. During this incubation, E. coli acquires mutations that are selected in response to this environment, ultimately leading to evolved populations that are better adapted to these complex conditions, which can lead to a better understanding of evolutionary mechanisms. Mutations in regulatory genes often play a role in adapting to heterogeneous environments. To identify such mutations, we examined transcriptional differences during log phase growth in unaged cells compared to those that had been aged for 10 days and regrown. We identified expression changes in genes involved in motility and chemotaxis after adaptation to long-term cultures. We hypothesized that aged populations would also have phenotypic changes in motility and that motility may play a role in survival and adaptation to long-term cultures. While aged populations did show an increase in motility, this increase was not essential for survival in long-term cultures. We identified mutations in the regulatory gene sspA and other genes that may contribute to the observed differences in motility. Taken together, these data provide an overall picture of the role of mutations in regulatory genes for adaptation while underscoring that all changes that occur during evolution in stressful environments are not necessarily adaptive. IMPORTANCE Understanding how bacteria adapt in long-term cultures aids in both better treatment options for bacterial infections and gives insight into the mechanisms involved in bacterial evolution. In the past, it has been difficult to study these organisms in their natural environments. By using experimental evolution in heterogeneous and stressful laboratory conditions, we can more closely mimic natural environments and examine evolutionary mechanisms. One way to observe these mechanisms is to look at transcriptomic and genomic data from cells adapted to these complex conditions. Here, we found that although aged cells increase motility, this increase is not essential for survival in these conditions. These data emphasize that not all changes that occur due to evolutionary processes are adaptive, but these observations could still lead to hypotheses about the causative mutations. The information gained here allow us to make inferences about general mechanisms underlying phenotypic changes due to evolution. 

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5. The roles of plasticity and evolutionary change in shaping gene expression variation in natural populations of extremophile fish

   https://doi.org/10.1111/mec.14360  

   Passow, Courtney N. ; Henpita, Chathurika ; Shaw, Jennifer H. ; Quackenbush, Corey R. ; Warren, Wesley C. ; Schartl, Manfred ; Arias‐Rodriguez, Lenin ; Kelley, Joanna L. ; Tobler, Michael ( October 2017 , Molecular Ecology)

   The notorious plasticity of gene expression responses and the complexity of environmental gradients complicate the identification of adaptive differences in gene regulation among populations. We combined transcriptome analyses in nature with common‐garden and exposure experiments to establish cause–effect relationships between the presence of a physiochemical stressor and expression differences, as well as to test how evolutionary change and plasticity interact to shape gene expression variation in natural systems. We studied two evolutionarily independent population pairs of an extremophile fish (Poecilia mexicana) living in toxic, hydrogen sulphide (H₂S)‐rich springs and adjacent nontoxic habitats and assessed genomewide expression patterns of wild‐caught and common‐garden‐raised individuals exposed to different concentrations of H₂S. We found that 7.7% of genes that were differentially expressed between sulphidic and nonsulphidic ecotypes remained differentially expressed in the laboratory, indicating that sources of selection other than H₂S—or plastic responses to other environmental factors—contribute substantially to gene expression patterns observed in the wild. Concordantly differentially expressed genes in the wild and the laboratory were primarily associated with H₂S detoxification, sulphur processing and metabolic physiology. While shared, ancestral plasticity played a minor role in shaping gene expression variation observed in nature, we documented evidence for evolved population differences in the constitutive expression as well as the H₂S inducibility of candidate genes. Mechanisms underlying gene expression variation also varied substantially across the two ecotype pairs. These results provide a springboard for studying evolutionary modifications of gene regulatory mechanisms that underlie expression variation in locally adapted populations.

    

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