Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes
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...
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| Format: | Article |
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eLife Sciences Publications Ltd
2025-02-01
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| Online Access: | https://elifesciences.org/articles/97764 |
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| author | Hope M Healey Hayden B Penn Clayton M Small Susan Bassham Vithika Goyal Micah A Woods William A Cresko |
| author_facet | Hope M Healey Hayden B Penn Clayton M Small Susan Bassham Vithika Goyal Micah A Woods William A Cresko |
| author_sort | Hope M Healey |
| collection | DOAJ |
| description | 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 genome assemblies revealed suggestive gene content differences and provided 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 the 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 that 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 the novelties of these fish evolved. |
| format | Article |
| id | doaj-art-bece49b5965242d8af1a45ec260fe1cf |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj-art-bece49b5965242d8af1a45ec260fe1cf2025-02-03T12:06:21ZengeLife Sciences Publications LtdeLife2050-084X2025-02-011310.7554/eLife.97764Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishesHope M Healey0https://orcid.org/0000-0001-9978-1553Hayden B Penn1https://orcid.org/0009-0000-3090-5423Clayton M Small2https://orcid.org/0000-0003-1615-7590Susan Bassham3https://orcid.org/0000-0002-7309-2095Vithika Goyal4https://orcid.org/0009-0009-8601-8474Micah A Woods5https://orcid.org/0009-0004-2156-3352William A Cresko6https://orcid.org/0000-0002-3496-8074Institute of Ecology and Evolution, University of Oregon, Eugene, United States; Knight Campus for Accelerating Scientific Impact, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United States; School of Computer and Data Science, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United StatesInstitute of Ecology and Evolution, University of Oregon, Eugene, United States; Knight Campus for Accelerating Scientific Impact, University of Oregon, Eugene, United StatesSeahorses, 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 genome assemblies revealed suggestive gene content differences and provided 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 the 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 that 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 the novelties of these fish evolved.https://elifesciences.org/articles/97764SyngnathidaescRNAseqevolutionary noveltynon-traditional modelevolution of developmentsyngnathid fishes |
| spellingShingle | Hope M Healey Hayden B Penn Clayton M Small Susan Bassham Vithika Goyal Micah A Woods William A Cresko Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes eLife Syngnathidae scRNAseq evolutionary novelty non-traditional model evolution of development syngnathid fishes |
| title | Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| title_full | Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| title_fullStr | Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| title_full_unstemmed | Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| title_short | Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| title_sort | single cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes |
| topic | Syngnathidae scRNAseq evolutionary novelty non-traditional model evolution of development syngnathid fishes |
| url | https://elifesciences.org/articles/97764 |
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