Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy
Abstract Background The Scalidophora (Kinorhyncha, Loricifera and Priapulida) have an important phylogenetic position as early branching ecdysozoans, yet the architecture of their nervous organ systems is notably underinvestigated. Without such information, and in the absence of a stable phylogeneti...
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| Format: | Article |
| Language: | English |
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BMC
2019-04-01
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| Series: | BMC Evolutionary Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12862-019-1405-4 |
| _version_ | 1818695212681134080 |
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| author | María Herranz Brian S. Leander Fernando Pardos Michael J. Boyle |
| author_facet | María Herranz Brian S. Leander Fernando Pardos Michael J. Boyle |
| author_sort | María Herranz |
| collection | DOAJ |
| description | Abstract Background The Scalidophora (Kinorhyncha, Loricifera and Priapulida) have an important phylogenetic position as early branching ecdysozoans, yet the architecture of their nervous organ systems is notably underinvestigated. Without such information, and in the absence of a stable phylogenetic context, we are inhibited from producing adequate hypotheses about the evolution and diversification of ecdysozoan nervous systems. Here, we utilize confocal laser scanning microscopy to characterize serotonergic, tubulinergic and FMRFamidergic immunoreactivity patterns in a comparative neuroanatomical study with three species of Echinoderes, the most speciose, abundant and diverse genus within Kinorhyncha. Results Neuroanatomy in Echinoderes as revealed by acetylated α-tubulin immunoreactivity includes a circumpharyngeal brain and ten neurite bundles in the head region that converge into five longitudinal nerves within the trunk. The ventral nerve cord is ganglionated, emerging from the brain with two connectives that converge in trunk segments 2–3, and diverge again within segment 8. The longitudinal nerves and ventral nerve cord are connected by two transverse neurites in segments 2–9. Differences among species correlate with the number, position and innervation of cuticular structures along the body. Patterns of serotoninergic and FMRFamidergic immunoreactivity correlate with the position of the brain neuropil and the ventral nerve cord. Distinct serotonergic and FMRFamidergic somata are associated with the brain neuropil and specific trunk segments along the ventral nerve cord. Conclusions Neural architecture is highly conserved across all three species, suggesting that our results reveal a pattern that is common to more than 40% of the species within Kinorhyncha. The nervous system of Echinoderes is segmented along most of the trunk; however, posterior trunk segments exhibit modifications that are likely associated with sensorial, motor or reproductive functions. Although all kinorhynchs show some evidence of an externally segmented trunk, it is unclear whether external segmentation matches internal segmentation of nervous and muscular organ systems across Kinorhyncha, as we observed in Echinoderes. The neuroanatomical data provided in this study not only expand the limited knowledge on kinorhynch nervous systems but also establish a comparative morphological framework within Scalidophora that will support broader inferences about the evolution of neural architecture among the deepest branching lineages of the Ecdysozoa. |
| first_indexed | 2024-12-17T13:41:53Z |
| format | Article |
| id | doaj.art-d7a818483384440695c2d116d063d40a |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-17T13:41:53Z |
| publishDate | 2019-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-d7a818483384440695c2d116d063d40a2022-12-21T21:46:15ZengBMCBMC Evolutionary Biology1471-21482019-04-0119112010.1186/s12862-019-1405-4Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopyMaría Herranz0Brian S. Leander1Fernando Pardos2Michael J. Boyle3Departments of Zoology and Botany, University of British Columbia. Biodiversity Research CentreDepartments of Zoology and Botany, University of British Columbia. Biodiversity Research CentreDepartamento de Biodiversidad, Ecología y EvoluciónSmithsonian Institution, Smithsonian Marine Station at Fort PierceAbstract Background The Scalidophora (Kinorhyncha, Loricifera and Priapulida) have an important phylogenetic position as early branching ecdysozoans, yet the architecture of their nervous organ systems is notably underinvestigated. Without such information, and in the absence of a stable phylogenetic context, we are inhibited from producing adequate hypotheses about the evolution and diversification of ecdysozoan nervous systems. Here, we utilize confocal laser scanning microscopy to characterize serotonergic, tubulinergic and FMRFamidergic immunoreactivity patterns in a comparative neuroanatomical study with three species of Echinoderes, the most speciose, abundant and diverse genus within Kinorhyncha. Results Neuroanatomy in Echinoderes as revealed by acetylated α-tubulin immunoreactivity includes a circumpharyngeal brain and ten neurite bundles in the head region that converge into five longitudinal nerves within the trunk. The ventral nerve cord is ganglionated, emerging from the brain with two connectives that converge in trunk segments 2–3, and diverge again within segment 8. The longitudinal nerves and ventral nerve cord are connected by two transverse neurites in segments 2–9. Differences among species correlate with the number, position and innervation of cuticular structures along the body. Patterns of serotoninergic and FMRFamidergic immunoreactivity correlate with the position of the brain neuropil and the ventral nerve cord. Distinct serotonergic and FMRFamidergic somata are associated with the brain neuropil and specific trunk segments along the ventral nerve cord. Conclusions Neural architecture is highly conserved across all three species, suggesting that our results reveal a pattern that is common to more than 40% of the species within Kinorhyncha. The nervous system of Echinoderes is segmented along most of the trunk; however, posterior trunk segments exhibit modifications that are likely associated with sensorial, motor or reproductive functions. Although all kinorhynchs show some evidence of an externally segmented trunk, it is unclear whether external segmentation matches internal segmentation of nervous and muscular organ systems across Kinorhyncha, as we observed in Echinoderes. The neuroanatomical data provided in this study not only expand the limited knowledge on kinorhynch nervous systems but also establish a comparative morphological framework within Scalidophora that will support broader inferences about the evolution of neural architecture among the deepest branching lineages of the Ecdysozoa.http://link.springer.com/article/10.1186/s12862-019-1405-4EcdysozoaNervous systemNerve cordMorphologyScalidophoraSegmentation |
| spellingShingle | María Herranz Brian S. Leander Fernando Pardos Michael J. Boyle Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy BMC Evolutionary Biology Ecdysozoa Nervous system Nerve cord Morphology Scalidophora Segmentation |
| title | Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy |
| title_full | Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy |
| title_fullStr | Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy |
| title_full_unstemmed | Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy |
| title_short | Neuroanatomy of mud dragons: a comprehensive view of the nervous system in Echinoderes (Kinorhyncha) by confocal laser scanning microscopy |
| title_sort | neuroanatomy of mud dragons a comprehensive view of the nervous system in echinoderes kinorhyncha by confocal laser scanning microscopy |
| topic | Ecdysozoa Nervous system Nerve cord Morphology Scalidophora Segmentation |
| url | http://link.springer.com/article/10.1186/s12862-019-1405-4 |
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