Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus
Comparative studies on the development of nervous systems have a significant impact on understanding animal nervous system evolution. Nevertheless, an important question is to what degree neuronal structures, which play an important role in early stages, become part of the adult nervous system or ar...
Saved in:
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-01-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2024.1439897/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1841543680860618752 |
|---|---|
| author | Anna Seybold Anna Seybold Suman Kumar Suman Kumar Sharat Chandra Tumu Harald Hausen Harald Hausen |
| author_facet | Anna Seybold Anna Seybold Suman Kumar Suman Kumar Sharat Chandra Tumu Harald Hausen Harald Hausen |
| author_sort | Anna Seybold |
| collection | DOAJ |
| description | Comparative studies on the development of nervous systems have a significant impact on understanding animal nervous system evolution. Nevertheless, an important question is to what degree neuronal structures, which play an important role in early stages, become part of the adult nervous system or are relevant for its formation. This is likely in many direct developers, but it is not the case in forms with catastrophic metamorphosis. It is not clear in many forms with gradual metamorphosis. This introduces uncertainty in tracing the evolution of nervous systems and of larval forms. One of the prominent larval characteristics of numerous planktonic marine organisms is the epidermal ciliation used for swimming and steering, which disappears during metamorphosis. Therefore, the neuronal elements controlling the ciliary beating are often assumed to vanish with the cilia and regarded as purely larval specializations. With volume EM, we followed the neuronal targets of the very first pioneer neurons at the apical and posterior ends of the larva of the annelid Malacoceros fuliginosus. We observed that all of these pioneers appear to have a dual function. Although they are laying the paths for the later adult nervous system, they also make synaptic contact with the main ciliated ring of the larva. We propose that the formation of the later adult nervous system and the innervation of the larval locomotory organ are indeed closely linked to each other. This has implications for understanding the early nervous system development of marine larvae and for existing hypotheses on nervous system evolution. |
| format | Article |
| id | doaj-art-42ca822bd4a443668a0ae55195973129 |
| institution | Kabale University |
| issn | 1662-453X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj-art-42ca822bd4a443668a0ae551959731292025-01-13T06:11:30ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2025-01-011810.3389/fnins.2024.14398971439897Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosusAnna Seybold0Anna Seybold1Suman Kumar2Suman Kumar3Sharat Chandra Tumu4Harald Hausen5Harald Hausen6Michael Sars Centre, University of Bergen, Bergen, NorwayInstitute of Zoology, University of Innsbruck, Innsbruck, AustriaMichael Sars Centre, University of Bergen, Bergen, NorwayDepartment of Biosciences, University of Oslo, Oslo, NorwayMichael Sars Centre, University of Bergen, Bergen, NorwayMichael Sars Centre, University of Bergen, Bergen, NorwayDepartment of Earth Sciences, University of Bergen, Bergen, NorwayComparative studies on the development of nervous systems have a significant impact on understanding animal nervous system evolution. Nevertheless, an important question is to what degree neuronal structures, which play an important role in early stages, become part of the adult nervous system or are relevant for its formation. This is likely in many direct developers, but it is not the case in forms with catastrophic metamorphosis. It is not clear in many forms with gradual metamorphosis. This introduces uncertainty in tracing the evolution of nervous systems and of larval forms. One of the prominent larval characteristics of numerous planktonic marine organisms is the epidermal ciliation used for swimming and steering, which disappears during metamorphosis. Therefore, the neuronal elements controlling the ciliary beating are often assumed to vanish with the cilia and regarded as purely larval specializations. With volume EM, we followed the neuronal targets of the very first pioneer neurons at the apical and posterior ends of the larva of the annelid Malacoceros fuliginosus. We observed that all of these pioneers appear to have a dual function. Although they are laying the paths for the later adult nervous system, they also make synaptic contact with the main ciliated ring of the larva. We propose that the formation of the later adult nervous system and the innervation of the larval locomotory organ are indeed closely linked to each other. This has implications for understanding the early nervous system development of marine larvae and for existing hypotheses on nervous system evolution.https://www.frontiersin.org/articles/10.3389/fnins.2024.1439897/fullnervous systemdevelopmentevolutionneural circuitryvolume electron microscopyAnnelida |
| spellingShingle | Anna Seybold Anna Seybold Suman Kumar Suman Kumar Sharat Chandra Tumu Harald Hausen Harald Hausen Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus Frontiers in Neuroscience nervous system development evolution neural circuitry volume electron microscopy Annelida |
| title | Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus |
| title_full | Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus |
| title_fullStr | Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus |
| title_full_unstemmed | Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus |
| title_short | Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus |
| title_sort | neurons with larval synaptic targets pioneer the later nervous system in the annelid malacoceros fuliginosus |
| topic | nervous system development evolution neural circuitry volume electron microscopy Annelida |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2024.1439897/full |
| work_keys_str_mv | AT annaseybold neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT annaseybold neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT sumankumar neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT sumankumar neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT sharatchandratumu neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT haraldhausen neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus AT haraldhausen neuronswithlarvalsynaptictargetspioneerthelaternervoussystemintheannelidmalacocerosfuliginosus |