The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae)
Abstract Background Enteropneusts are benthic marine invertebrates that belong to the deuterostome phylum Hemichordata. The two main clades of enteropneusts are defined by differences in early life history strategies. In the Spengelidae and Ptychoderidae, development is indirect via a planktotrophic...
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| Format: | Article |
| Language: | English |
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BMC
2018-06-01
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| Series: | Frontiers in Zoology |
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| Online Access: | http://link.springer.com/article/10.1186/s12983-018-0270-0 |
| _version_ | 1811310169866371072 |
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| author | Paul Gonzalez Jeffrey Z. Jiang Christopher J. Lowe |
| author_facet | Paul Gonzalez Jeffrey Z. Jiang Christopher J. Lowe |
| author_sort | Paul Gonzalez |
| collection | DOAJ |
| description | Abstract Background Enteropneusts are benthic marine invertebrates that belong to the deuterostome phylum Hemichordata. The two main clades of enteropneusts are defined by differences in early life history strategies. In the Spengelidae and Ptychoderidae, development is indirect via a planktotrophic tornaria larva. In contrast, development in the Harrimanidae is direct without an intervening larval life history stage. Most molecular studies in the development and evolution of the enteropneust adult body plan have been carried out in the harrimanid Saccoglossus kowalevskii. In order to compare these two developmental strategies, we have selected the spengelid enteropneust Schizocardium californicum as a suitable indirect developing species for molecular developmental studies. Here we describe the methods for adult collecting, spawning and larval rearing in Schizocardium californicum, and describe embryogenesis, larval development, and metamorphosis, using light microscopy, immunocytochemistry and confocal microscopy. Results Adult reproductive individuals can be collected intertidally and almost year-round. Spawning can be triggered by heat shock and large numbers of larvae can be reared through metamorphosis under laboratory conditions. Gastrulation begins at 17 h post-fertilization (hpf) and embryos hatch at 26 hpf as ciliated gastrulae. At 3 days post-fertilization (dpf), the tornaria has a circumoral ciliary band, mouth, tripartite digestive tract, protocoel, larval muscles and a simple serotonergic nervous system. The telotroch develops at 5 dpf. In the course of 60 days, the serotonergic nervous system becomes more elaborate, the posterior coeloms develop, and the length of the circumoral ciliary band increases. At the end of the larval stage, larval muscles disappear, gill slits form, and adult muscles develop. Metamorphosis occurs spontaneously when the larva reaches its maximal size (ca. 3 mm), and involves loss and reorganization of larval structures (muscles, nervous system, digestive tract), as well as development of adult structures (adult muscles, tripartite body organization). Conclusions This study will enable future research in S. californicum to address long standing questions related to the evolution of axial patterning mechanisms, germ layer induction, neurogenesis and neural patterning, the mechanisms of metamorphosis, the relationships between larval and adult body plans, and the evolution of metazoan larval forms. |
| first_indexed | 2024-04-13T09:54:41Z |
| format | Article |
| id | doaj.art-48b42e2a1fa341c9ab0f8094e754b92d |
| institution | Directory Open Access Journal |
| issn | 1742-9994 |
| language | English |
| last_indexed | 2024-04-13T09:54:41Z |
| publishDate | 2018-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Frontiers in Zoology |
| spelling | doaj.art-48b42e2a1fa341c9ab0f8094e754b92d2022-12-22T02:51:29ZengBMCFrontiers in Zoology1742-99942018-06-0115112410.1186/s12983-018-0270-0The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae)Paul Gonzalez0Jeffrey Z. Jiang1Christopher J. Lowe2Hopkins Marine Station, Department of Biology, Stanford UniversityDepartment of Chemistry, University of PennsylvaniaHopkins Marine Station, Department of Biology, Stanford UniversityAbstract Background Enteropneusts are benthic marine invertebrates that belong to the deuterostome phylum Hemichordata. The two main clades of enteropneusts are defined by differences in early life history strategies. In the Spengelidae and Ptychoderidae, development is indirect via a planktotrophic tornaria larva. In contrast, development in the Harrimanidae is direct without an intervening larval life history stage. Most molecular studies in the development and evolution of the enteropneust adult body plan have been carried out in the harrimanid Saccoglossus kowalevskii. In order to compare these two developmental strategies, we have selected the spengelid enteropneust Schizocardium californicum as a suitable indirect developing species for molecular developmental studies. Here we describe the methods for adult collecting, spawning and larval rearing in Schizocardium californicum, and describe embryogenesis, larval development, and metamorphosis, using light microscopy, immunocytochemistry and confocal microscopy. Results Adult reproductive individuals can be collected intertidally and almost year-round. Spawning can be triggered by heat shock and large numbers of larvae can be reared through metamorphosis under laboratory conditions. Gastrulation begins at 17 h post-fertilization (hpf) and embryos hatch at 26 hpf as ciliated gastrulae. At 3 days post-fertilization (dpf), the tornaria has a circumoral ciliary band, mouth, tripartite digestive tract, protocoel, larval muscles and a simple serotonergic nervous system. The telotroch develops at 5 dpf. In the course of 60 days, the serotonergic nervous system becomes more elaborate, the posterior coeloms develop, and the length of the circumoral ciliary band increases. At the end of the larval stage, larval muscles disappear, gill slits form, and adult muscles develop. Metamorphosis occurs spontaneously when the larva reaches its maximal size (ca. 3 mm), and involves loss and reorganization of larval structures (muscles, nervous system, digestive tract), as well as development of adult structures (adult muscles, tripartite body organization). Conclusions This study will enable future research in S. californicum to address long standing questions related to the evolution of axial patterning mechanisms, germ layer induction, neurogenesis and neural patterning, the mechanisms of metamorphosis, the relationships between larval and adult body plans, and the evolution of metazoan larval forms.http://link.springer.com/article/10.1186/s12983-018-0270-0EnteropneustaHemichordataIndirect developmentMetamorphosisPlanktotrophySchizocardium californicum |
| spellingShingle | Paul Gonzalez Jeffrey Z. Jiang Christopher J. Lowe The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) Frontiers in Zoology Enteropneusta Hemichordata Indirect development Metamorphosis Planktotrophy Schizocardium californicum |
| title | The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) |
| title_full | The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) |
| title_fullStr | The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) |
| title_full_unstemmed | The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) |
| title_short | The development and metamorphosis of the indirect developing acorn worm Schizocardium californicum (Enteropneusta: Spengelidae) |
| title_sort | development and metamorphosis of the indirect developing acorn worm schizocardium californicum enteropneusta spengelidae |
| topic | Enteropneusta Hemichordata Indirect development Metamorphosis Planktotrophy Schizocardium californicum |
| url | http://link.springer.com/article/10.1186/s12983-018-0270-0 |
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