Convergent evolution of the sensory pits in and within flatworms
Abstract Background Unlike most free-living platyhelminths, catenulids, the sister group to all remaining flatworms, do not have eyes. Instead, the most prominent sensory structures in their heads are statocysts or sensory pits. The latter, found in the family Stenostomidae, are concave depressions...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01768-y |
| _version_ | 1797451487206440960 |
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| author | Ludwik Gąsiorowski Isabel Lucia Dittmann Jeremias N. Brand Torben Ruhwedel Wiebke Möbius Bernhard Egger Jochen C. Rink |
| author_facet | Ludwik Gąsiorowski Isabel Lucia Dittmann Jeremias N. Brand Torben Ruhwedel Wiebke Möbius Bernhard Egger Jochen C. Rink |
| author_sort | Ludwik Gąsiorowski |
| collection | DOAJ |
| description | Abstract Background Unlike most free-living platyhelminths, catenulids, the sister group to all remaining flatworms, do not have eyes. Instead, the most prominent sensory structures in their heads are statocysts or sensory pits. The latter, found in the family Stenostomidae, are concave depressions located laterally on the head that represent one of the taxonomically important traits of the family. In the past, the sensory pits of flatworms have been homologized with the cephalic organs of nemerteans, a clade that occupies a sister position to platyhelminths in some recent phylogenies. To test for this homology, we studied morphology and gene expression in the sensory pits of the catenulid Stenostomum brevipharyngium. Results We used confocal and electron microscopy to investigate the detailed morphology of the sensory pits, as well as their formation during regeneration and asexual reproduction. The most prevalent cell type within the organ is epidermally-derived neuron-like cells that have cell bodies embedded deeply in the brain lobes and long neurite-like processes extending to the bottom of the pit. Those elongated processes are adorned with extensive microvillar projections that fill up the cavity of the pit, but cilia are not associated with the sensory pit. We also studied the expression patterns of some of the transcription factors expressed in the nemertean cephalic organs during the development of the pits. Only a single gene, pax4/6, is expressed in both the cerebral organs of nemerteans and sensory pits of S. brevipharyngium, challenging the idea of their deep homology. Conclusions Since there is no morphological or molecular correspondence between the sensory pits of Stenostomum and the cerebral organs of nemerteans, we reject their homology. Interestingly, the major cell type contributing to the sensory pits of stenostomids shows ultrastructural similarities to the rhabdomeric photoreceptors of other flatworms and expresses ortholog of the gene pax4/6, the pan-bilaterian master regulator of eye development. We suggest that the sensory pits of stenostomids might have evolved from the ancestral rhabdomeric photoreceptors that lost their photosensitivity and evolved secondary function. The mapping of head sensory structures on plathelminth phylogeny indicates that sensory pit-like organs evolved many times independently in flatworms. |
| first_indexed | 2024-03-09T14:55:22Z |
| format | Article |
| id | doaj.art-8bb1665bc53141d1ae44c1c81afdf4fb |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-09T14:55:22Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-8bb1665bc53141d1ae44c1c81afdf4fb2023-11-26T14:14:25ZengBMCBMC Biology1741-70072023-11-0121111910.1186/s12915-023-01768-yConvergent evolution of the sensory pits in and within flatwormsLudwik Gąsiorowski0Isabel Lucia Dittmann1Jeremias N. Brand2Torben Ruhwedel3Wiebke Möbius4Bernhard Egger5Jochen C. Rink6Department of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesInstitut Für Zoologie, Universität InnsbruckDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesElectron Microscopy Facility, Department of Neurogenetics, Max Planck Institute for Multidisciplinary SciencesElectron Microscopy Facility, Department of Neurogenetics, Max Planck Institute for Multidisciplinary SciencesInstitut Für Zoologie, Universität InnsbruckDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesAbstract Background Unlike most free-living platyhelminths, catenulids, the sister group to all remaining flatworms, do not have eyes. Instead, the most prominent sensory structures in their heads are statocysts or sensory pits. The latter, found in the family Stenostomidae, are concave depressions located laterally on the head that represent one of the taxonomically important traits of the family. In the past, the sensory pits of flatworms have been homologized with the cephalic organs of nemerteans, a clade that occupies a sister position to platyhelminths in some recent phylogenies. To test for this homology, we studied morphology and gene expression in the sensory pits of the catenulid Stenostomum brevipharyngium. Results We used confocal and electron microscopy to investigate the detailed morphology of the sensory pits, as well as their formation during regeneration and asexual reproduction. The most prevalent cell type within the organ is epidermally-derived neuron-like cells that have cell bodies embedded deeply in the brain lobes and long neurite-like processes extending to the bottom of the pit. Those elongated processes are adorned with extensive microvillar projections that fill up the cavity of the pit, but cilia are not associated with the sensory pit. We also studied the expression patterns of some of the transcription factors expressed in the nemertean cephalic organs during the development of the pits. Only a single gene, pax4/6, is expressed in both the cerebral organs of nemerteans and sensory pits of S. brevipharyngium, challenging the idea of their deep homology. Conclusions Since there is no morphological or molecular correspondence between the sensory pits of Stenostomum and the cerebral organs of nemerteans, we reject their homology. Interestingly, the major cell type contributing to the sensory pits of stenostomids shows ultrastructural similarities to the rhabdomeric photoreceptors of other flatworms and expresses ortholog of the gene pax4/6, the pan-bilaterian master regulator of eye development. We suggest that the sensory pits of stenostomids might have evolved from the ancestral rhabdomeric photoreceptors that lost their photosensitivity and evolved secondary function. The mapping of head sensory structures on plathelminth phylogeny indicates that sensory pit-like organs evolved many times independently in flatworms.https://doi.org/10.1186/s12915-023-01768-yRegenerationParatomyAsexual reproductionRhabdomeric photoreceptorsMorphologySpiralia |
| spellingShingle | Ludwik Gąsiorowski Isabel Lucia Dittmann Jeremias N. Brand Torben Ruhwedel Wiebke Möbius Bernhard Egger Jochen C. Rink Convergent evolution of the sensory pits in and within flatworms BMC Biology Regeneration Paratomy Asexual reproduction Rhabdomeric photoreceptors Morphology Spiralia |
| title | Convergent evolution of the sensory pits in and within flatworms |
| title_full | Convergent evolution of the sensory pits in and within flatworms |
| title_fullStr | Convergent evolution of the sensory pits in and within flatworms |
| title_full_unstemmed | Convergent evolution of the sensory pits in and within flatworms |
| title_short | Convergent evolution of the sensory pits in and within flatworms |
| title_sort | convergent evolution of the sensory pits in and within flatworms |
| topic | Regeneration Paratomy Asexual reproduction Rhabdomeric photoreceptors Morphology Spiralia |
| url | https://doi.org/10.1186/s12915-023-01768-y |
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