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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. The effect of E93 knockdown on female reproduction in the red flour beetle, Tribolium castaneum

   https://doi.org/10.1002/arch.21688  

   Eid, Duaa Musleh ; Chereddy, Shankar C. R. R. ; Palli, Subba Reddy ( May 2020 , Archives of Insect Biochemistry and Physiology)

   The E93 transcription factor is a member of helix‐turn‐helix transcription factor family containing a Pip‐squeak motif. This ecdysone primary response gene was identified as a regulator of cell death inDrosophila melanogasterwhere it is involved in ecdysone‐induced autophagy and caspase activity that mediate degeneration of larval tissues during metamorphosis from larva to pupa. However, its function in adult insects is not well studied. To study E93 function in the red flour beetle,Tribolium castaneum, double‐stranded RNA (dsRNA) targeting E93 (dsE93) was injected into newly emerged adults. Knockdown of E93 caused a decrease in the synthesis of vitellogenin (Vg), oocyte development, and egg‐laying. Sequencing of RNA isolated from adults injected with dsE93 and controldsmalE(dsRNA targetingEscherichia coli malEgene) followed by differential gene expression analysis showed upregulation of genes involved in the metabolism of reserved nutrients.E93knockdown induced changes in gene expression resulted in a decrease in Vg synthesis in the fat body and oocyte maturation in ovaries. Mating experiments showed that females injected with dsE93 did not lay eggs. Knockdown ofE93caused a reduction in the number and size of lipid droplets in the fat body when compared with that in control beetles injected withdsmalE. These data suggest that during the first 2–3 days after the emergence of adult females, E93 suppresses genes coding for enzymes that metabolize reserved nutrients until initiation of vitellogenesis and oogenesis.

    

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3. The Makorin lep-2 and the lncRNA lep-5 regulate lin-28 to schedule sexual maturation of the C. elegans nervous system

   https://doi.org/10.7554/eLife.43660  

   Lawson, Hannah ; Vuong, Edward ; Miller, Renee M ; Kiontke, Karin ; Fitch, David HA ; Portman, Douglas S ( July 2019 , eLife)

   Most animals develop from juveniles, which cannot reproduce, to sexually mature adults. The most obvious signs of this transition are changes in body shape and size. However, changes also take place in the brain that enable the animals to adapt their behavior to the demands of adulthood. For example, fully fed adult male roundworms will leave a food source to search for mates, whereas juvenile males will continue feeding. The transition to sexual maturity needs to be carefully timed. Too early, and the animal risks compromising key stages of development. Too late, and the animal may be less competitive in the quest for reproductive success. Cues in the environment, such as the presence of food and mates, interact with timing mechanisms in the brain to trigger sexual maturity. But how these mechanisms work – in particular where and how an animal keeps track of its developmental stage – is not well understood. In the roundworm species Caenorhabditis elegans, waves of gene activity, known collectively as the heterochronic pathway, determine patterns of cell growth as animals mature. Through further studies of these worms, Lawson et al. now show that these waves also control the time at which neural circuits mature. In addition, the waves of activity occur inside the nervous system itself, rather than in a tissue that sends signals to the nervous system. Moreover, they occur independently inside many different neurons. Each neuron thus has its own molecular clock for keeping track of development. Several of the genes critical for developmental timekeeping in worms are also found in mammals, including two genes that help to control when puberty starts in humans. If one of these genes – called MKRN3 – does not work correctly, it can lead to a condition that causes individuals to go through puberty several years earlier than normal. Studying the mechanisms identified in roundworms may help us to better understand this disorder. More generally, future work that builds on the results presented by Lawson et al. will help to reveal how environmental cues and gene activity interact to control when we become adults. 

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4. 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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5. Extensive loss of Wnt genes in Tardigrada

   https://doi.org/10.1186/s12862-021-01954-y  

   Chavarria, Raul A. ; Game, Mandy ; Arbelaez, Briana ; Ramnarine, Chloe ; Snow, Zachary K. ; Smith, Frank W. ( December 2021 , BMC Ecology and Evolution)

   Wnt genes code for ligands that activate signaling pathways during development in Metazoa. Through the canonical Wnt (cWnt) signaling pathway, these genes regulate important processes in bilaterian development, such as establishing the anteroposterior axis and posterior growth. In Arthropoda, Wnt ligands also regulate segment polarity, and outgrowth and patterning of developing appendages. Arthropods are part of a lineage called Panarthropoda that includes Onychophora and Tardigrada. Previous studies revealed potential roles of Wnt genes in regulating posterior growth, segment polarity, and growth and patterning of legs in Onychophora. Unlike most other panarthropods, tardigrades lack posterior growth, but retain segmentation and appendages. Here, we investigated Wnt genes in tardigrades to gain insight into potential roles that these genes play during development of the highly compact and miniaturized tardigrade body plan.

   We analyzed published genomes for two representatives of Tardigrada,Hypsibius exemplarisandRamazzottius varieornatus. We identified single orthologs ofWnt4,Wnt5,Wnt9,Wnt11, andWntA, as well as twoWnt16paralogs in both tardigrade genomes. We only found aWnt2ortholog inH. exemplaris. We could not identify orthologs ofWnt1,Wnt6,Wnt7,Wnt8, orWnt10. We identified most other components of cWnt signaling in both tardigrade genomes. However, we were unable to identify an ortholog ofarrow/Lrp5/6, a gene that codes for a Frizzled co-receptor of Wnt ligands. Additionally, we found that some other animals that have lost several Wnt genes and are secondarily miniaturized, like tardigrades, are also missing an ortholog ofarrow/Lrp5/6. We analyzed the embryonic expression patterns of Wnt genes inH. exemplarisduring developmental stages that span the establishment of the AP axis through segmentation and leg development. We detected expression of all Wnt genes inH. exemplarisbesides one of theWnt16paralogs. During embryo elongation, expression of several Wnt genes was restricted to the posterior pole or a region between the anterior and posterior poles. Wnt genes were expressed in distinct patterns during segmentation and development of legs inH. exemplaris, rather than in broadly overlapping patterns.

   Our results indicate that Wnt signaling has been highly modified in Tardigrada. While most components of cWnt signaling are conserved in tardigrades, we conclude that tardigrades have lostWnt1,Wnt6,Wnt7,Wnt8, andWnt10, along witharrow/Lrp5/6. Our expression data may indicate a conserved role of Wnt genes in specifying posterior identities during establishment of the AP axis. However, the loss of several Wnt genes and the distinct expression patterns of Wnt genes during segmentation and leg development may indicate that combinatorial interactions among Wnt genes are less important during tardigrade development compared to many other animals. Based on our results, and comparisons to previous studies, we speculate that the loss of several Wnt genes in Tardigrada may be related to a reduced number of cells and simplified development that accompanied miniaturization and anatomical simplification in this lineage.

    

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