Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae)
Abstract Background Ramisyllis kingghidorahi (Annelida, Syllidae) is one of few annelid species with a ramified body, one anterior end and hundreds of posterior ends. R. kingghidorahi belongs to the family Syllidae, whose members reproduce by forming stolons, small autonomous reproductive units, at...
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2025-04-01
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| Online Access: | https://doi.org/10.1186/s12864-025-11587-w |
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| author | Guillermo Ponz-Segrelles Thilo Schulze Kohei Oguchi Daisuke S. Sato Mayuko Nakamura Yoshinobu Hayashi Christopher J. Glasby Toru Miura M. Teresa Aguado |
| author_facet | Guillermo Ponz-Segrelles Thilo Schulze Kohei Oguchi Daisuke S. Sato Mayuko Nakamura Yoshinobu Hayashi Christopher J. Glasby Toru Miura M. Teresa Aguado |
| author_sort | Guillermo Ponz-Segrelles |
| collection | DOAJ |
| description | Abstract Background Ramisyllis kingghidorahi (Annelida, Syllidae) is one of few annelid species with a ramified body, one anterior end and hundreds of posterior ends. R. kingghidorahi belongs to the family Syllidae, whose members reproduce by forming stolons, small autonomous reproductive units, at the posterior end. Molecular mechanisms controlling sexual reproduction are still poorly understood, but previous studies support an important role of the anterior end and stolons. The roles of different body regions during sexual reproduction in a complex branched body where there is only one head but multiple posterior ends, which develop hundreds of simultaneous stolons, have never been investigated. Consequently, we aimed to research the transcriptomic basis of sexual maturation and stolonization in R. kingghidorahi by performing differential gene expression analyses. Results Transcriptomes were assembled from different body regions (anterior end, midbody, and stolons) of male, female, and non-reproductive individuals. Comparative analyses revealed that body region had a greater impact on gene expression profiles than sex, with the anterior end and stolons showing extensive gene upregulation. Across-sex comparisons revealed sex-specific processes in all body regions, with stolons exhibiting the most differences in differential expression, likely related to gametogenesis and external sexual dimorphism. Fewer genes than expected were differentially expressed in the anterior region, a result for which different possible explanations are discussed. Surprisingly, key genes typically associated with segmentation and metamorphosis, such as Wnt and Hox, showed little differential expression, aligning with recent findings that stolon segments lack a specific segment identity. Conclusions This study presents the first transcriptomic data for a branched annelid species and offers new insights into the complex genetic regulation of reproduction in R. kingghidorahi. Additionally, it provides the first glimpse into the mechanisms of sexual maturation in branched syllids, which must coordinate stolonization across multiple posterior ends. These findings enhance our understanding of annelid reproductive biology and highlight the need for further research to uncover the physiological and molecular pathways regulating sexual maturation and stolonization in syllids and other annelids. |
| format | Article |
| id | doaj-art-30d2c354cb5d41ea8a9df51f0af4a992 |
| institution | OA Journals |
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| language | English |
| publishDate | 2025-04-01 |
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| spelling | doaj-art-30d2c354cb5d41ea8a9df51f0af4a9922025-08-20T02:30:20ZengBMCBMC Genomics1471-21642025-04-0126111710.1186/s12864-025-11587-wSex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae)Guillermo Ponz-Segrelles0Thilo Schulze1Kohei Oguchi2Daisuke S. Sato3Mayuko Nakamura4Yoshinobu Hayashi5Christopher J. Glasby6Toru Miura7M. Teresa Aguado8IES El Burgo-Ignacio-EcheverríaAnimal Evolution & Biodiversity, Georg-August-Universität GöttingenMisaki Marine Biological Station, School of Science, The University of TokyoMisaki Marine Biological Station, School of Science, The University of TokyoMisaki Marine Biological Station, School of Science, The University of TokyoDepartment of Biology, Keio UniversityMuseum and Art Gallery of the Northern TerritoryMisaki Marine Biological Station, School of Science, The University of TokyoAnimal Evolution & Biodiversity, Georg-August-Universität GöttingenAbstract Background Ramisyllis kingghidorahi (Annelida, Syllidae) is one of few annelid species with a ramified body, one anterior end and hundreds of posterior ends. R. kingghidorahi belongs to the family Syllidae, whose members reproduce by forming stolons, small autonomous reproductive units, at the posterior end. Molecular mechanisms controlling sexual reproduction are still poorly understood, but previous studies support an important role of the anterior end and stolons. The roles of different body regions during sexual reproduction in a complex branched body where there is only one head but multiple posterior ends, which develop hundreds of simultaneous stolons, have never been investigated. Consequently, we aimed to research the transcriptomic basis of sexual maturation and stolonization in R. kingghidorahi by performing differential gene expression analyses. Results Transcriptomes were assembled from different body regions (anterior end, midbody, and stolons) of male, female, and non-reproductive individuals. Comparative analyses revealed that body region had a greater impact on gene expression profiles than sex, with the anterior end and stolons showing extensive gene upregulation. Across-sex comparisons revealed sex-specific processes in all body regions, with stolons exhibiting the most differences in differential expression, likely related to gametogenesis and external sexual dimorphism. Fewer genes than expected were differentially expressed in the anterior region, a result for which different possible explanations are discussed. Surprisingly, key genes typically associated with segmentation and metamorphosis, such as Wnt and Hox, showed little differential expression, aligning with recent findings that stolon segments lack a specific segment identity. Conclusions This study presents the first transcriptomic data for a branched annelid species and offers new insights into the complex genetic regulation of reproduction in R. kingghidorahi. Additionally, it provides the first glimpse into the mechanisms of sexual maturation in branched syllids, which must coordinate stolonization across multiple posterior ends. These findings enhance our understanding of annelid reproductive biology and highlight the need for further research to uncover the physiological and molecular pathways regulating sexual maturation and stolonization in syllids and other annelids.https://doi.org/10.1186/s12864-025-11587-wGemmiparitySexual maturationReproductionSchizogamyComparative transcriptomicsAnnelid physiology |
| spellingShingle | Guillermo Ponz-Segrelles Thilo Schulze Kohei Oguchi Daisuke S. Sato Mayuko Nakamura Yoshinobu Hayashi Christopher J. Glasby Toru Miura M. Teresa Aguado Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) BMC Genomics Gemmiparity Sexual maturation Reproduction Schizogamy Comparative transcriptomics Annelid physiology |
| title | Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) |
| title_full | Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) |
| title_fullStr | Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) |
| title_full_unstemmed | Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) |
| title_short | Sex-specific differential gene expression during stolonization in the branching syllid Ramisyllis kingghidorahi (Annelida, Syllidae) |
| title_sort | sex specific differential gene expression during stolonization in the branching syllid ramisyllis kingghidorahi annelida syllidae |
| topic | Gemmiparity Sexual maturation Reproduction Schizogamy Comparative transcriptomics Annelid physiology |
| url | https://doi.org/10.1186/s12864-025-11587-w |
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