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1. Transcriptomic evidence for visual adaptation during the aquatic to terrestrial metamorphosis in leopard frogs

   https://doi.org/10.1186/s12915-022-01341-z  

   Schott, Ryan K. ; Bell, Rayna C. ; Loew, Ellis R. ; Thomas, Kate N. ; Gower, David J. ; Streicher, Jeffrey W. ; Fujita, Matthew K. ( June 2022 , BMC Biology)

   Differences in morphology, ecology, and behavior through ontogeny can result in opposing selective pressures at different life stages. Most animals, however, transition through two or more distinct phenotypic phases, which is hypothesized to allow each life stage to adapt more freely to its ecological niche. How this applies to sensory systems, and in particular how sensory systems adapt across life stages at the molecular level, is not well understood. Here, we used whole-eye transcriptomes to investigate differences in gene expression between tadpole and juvenile southern leopard frogs (Lithobates sphenocephalus), which rely on vision in aquatic and terrestrial light environments, respectively. Because visual physiology changes with light levels, we also tested the effect of light and dark exposure.

   We found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles and 5% for light/dark exposure. Analyses targeting a curated subset of visual genes revealed significant differential expression of genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments.

   Overall, we identified extensive expression-level differences in the eyes of tadpoles and juveniles related to observed morphological and physiological changes through metamorphosis and corresponding adaptive shifts to improve vision in the distinct aquatic and terrestrial light environments these frogs inhabit during their life cycle. More broadly, these results suggest that decoupling of gene expression can mediate the opposing selection pressures experienced by organisms with complex life cycles that inhabit different environmental conditions throughout ontogeny.

    

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2. Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration

   https://doi.org/10.1186/s12864-023-09839-8  

   Burghardt, Emily ; Rakijas, Jessica ; Tyagi, Antariksh ; Majumder, Pralay ; Olson, Bradley J. S. C. ; McDonald, Jocelyn A. ( December 2023 , BMC Genomics)

   Collective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis,Drosophilaborder cells undergo collective migration. Border cells round up into a small group at the pre-migration stage, detach from the epithelium and undergo a dynamic and highly regulated migration at the mid-migration stage, and stop at the oocyte, their final destination, at the post-migration stage. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct active phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration.

   We performed RNA-sequencing on border cells isolated at pre-, mid-, and post-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also uncovered a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated the in vivo expression and function of a subset of identified genes in border cells.

   Overall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues.

    

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3. Stage- and sex-specific transcriptome analyses reveal distinctive sensory gene expression patterns in a butterfly

   https://doi.org/10.1186/s12864-021-07819-4  

   Ernst, David A. ; Westerman, Erica L. ( August 2021 , BMC Genomics)

   Animal behavior is largely driven by the information that animals are able to extract and process from their environment. However, the function and organization of sensory systems often change throughout ontogeny, particularly in animals that undergo indirect development. As an initial step toward investigating these ontogenetic changes at the molecular level, we characterized the sensory gene repertoire and examined the expression profiles of genes linked to vision and chemosensation in two life stages of an insect that goes through metamorphosis, the butterflyBicyclus anynana.

   Using RNA-seq, we compared gene expression in the heads of late fifth instar larvae and newly eclosed adults that were reared under identical conditions. Over 50 % of all expressed genes were differentially expressed between the two developmental stages, with 4,036 genes upregulated in larval heads and 4,348 genes upregulated in adult heads. In larvae, upregulated vision-related genes were biased toward those involved with eye development, while phototransduction genes dominated the vision genes that were upregulated in adults. Moreover, the majority of the chemosensory genes we identified in theB. anynanagenome were differentially expressed between larvae and adults, several of which share homology with genes linked to pheromone detection, host plant recognition, and foraging in other species of Lepidoptera.

   These results revealed promising candidates for furthering our understanding of sensory processing and behavior in the disparate developmental stages of butterflies and other animals that undergo metamorphosis.

    

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4. 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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5. Differential DNA methylation across environments has no effect on gene expression in the eastern oyster

   https://doi.org/10.1111/1365-2656.13645  

   Johnson, Kevin M. ; Sirovy, Kyle A. ; Kelly, Morgan W. ( December 2021 , Journal of Animal Ecology)

   It has been hypothesized that environmentally induced changes to gene body methylation could facilitate adaptive transgenerational responses to changing environments.

   We compared patterns of global gene expression (Tag‐seq) and gene body methylation (reduced representation bisulfite sequencing) in 80 eastern oystersCrassostrea virginicafrom six full‐sib families, common gardened for 14 months at two sites in the northern Gulf of Mexico that differed in mean salinity.

   At the time of sampling, oysters from the two sites differed in mass by 60% and in parasite loads by nearly two orders of magnitude. They also differentially expressed 35% of measured transcripts. However, we observed differential methylation at only 1.4% of potentially methylated loci in comparisons between individuals from these different environments, and little correspondence between differential methylation and differential gene expression.

   Instead, methylation patterns were largely driven by genetic differences among families, with a PERMANOVA analysis indicating nearly a two orders of magnitude greater number of genes differentially methylated between families than between environments.

   An analysis of CpG observed/expected values (CpG O/E) across theC.virginicagenome showed a distinct bimodal distribution, with genes from the first cluster showing the lower CpG O/E values, greater methylation and higher and more stable gene expression, while genes from the second cluster showed lower methylation, and lower and more variable gene expression.

   Taken together, the differential methylation results suggest that only a small portion of theC.virginicagenome is affected by environmentally induced changes in methylation. At this point, there is little evidence to suggest that environmentally induced methylation states would play a leading role in regulating gene expression responses to new environments.

    

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