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Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genomes revealed suggestive gene content differences and provide the opportunity for detailed genetic analyses. We created a single cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor.Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how their novelties evolved.
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Genetic, morphometric, and molecular analyses of interspecies differences in head shape and hybrid developmental defects in the wasp genus Nasonia
Abstract Males in the parasitoid wasp genus Nasonia have distinct, species-specific, head shapes. The availability of fertile hybrids among the species, along with obligate haploidy of males, facilitates analysis of complex gene interactions in development and evolution. Previous analyses showed that both the divergence in head shape between Nasonia vitripennis and Nasonia giraulti, and the head-specific developmental defects of F2 haploid hybrid males, are governed by multiple changes in networks of interacting genes. Here, we extend our understanding of the gene interactions that affect morphogenesis in male heads. Use of artificial diploid male hybrids shows that alleles mediating developmental defects are recessive, while there are diverse dominance relationships among other head shape traits. At the molecular level, the sex determination locus doublesex plays a major role in male head shape differences, but it is not the only important factor. Introgression of a giraulti region on chromsome 2 reveals a recessive locus that causes completely penetrant head clefting in both males and females in a vitripennis background. Finally, a third species (N. longicornis) was used to investigate the timing of genetic changes related to head morphology, revealing that most changes causing defects arose after the divergence of N. vitripennis from the other species, but prior to the divergence of N. giraulti and N. longicornis from each other. Our results demonstrate that developmental gene networks can be dissected using interspecies crosses in Nasonia, and set the stage for future fine-scale genetic dissection of both head shape and hybrid developmental defects.
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- PAR ID:
- 10309642
- Editor(s):
- Lott, S
- Date Published:
- Journal Name:
- G3 Genes|Genomes|Genetics
- Volume:
- 11
- Issue:
- 12
- ISSN:
- 2160-1836
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract CRISPR/Cas9 gene editing is a powerful technology to study the genetics of rising model organisms, such as the jewel waspNasonia vitripennis. However, current methods involving embryonic microinjection of CRISPR reagents are challenging. Delivery of Cas9 ribonucleoprotein into female ovaries is an alternative that has only been explored in a small handful of insects, such as mosquitoes, whiteflies and beetles. Here, we developed a simple protocol for germline gene editing by injecting Cas9 ribonucleoprotein in adultN. vitripennisfemales using either ReMOT control (Receptor‐Mediated Ovary Transduction of Cargo) or BAPC (Branched Amphiphilic Peptide Capsules) as ovary delivery methods. For ReMOT Control we used theDrosophila melanogaster‐derived peptide ‘P2C’ fused to EGFP to visualize the ovary delivery, and fused to Cas9 protein for gene editing of thecinnabargene using saponin as an endosomal escape reagent. For BAPC we optimized the concentrations of protein, sgRNA and the transfection reagent. We demonstrate delivery of protein cargo such as EGFP and Cas9 into developing oocytes via P2C peptide and BAPC. Additionally, somatic and germline gene editing were demonstrated. This approach will greatly facilitate CRISPR‐applied genetic manipulation in this and other rising model organisms.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/g3journal/jkab313
