From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra
Abstract Background With more than 30,000 species, teleosts comprise about half of today’s living vertebrates, enriched with a wide set of adaptations to all aquatic systems. Their evolution was marked by modifications of their tail, that involved major rearrangements of the metameric organization o...
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| Format: | Article |
| Language: | English |
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BMC
2020-06-01
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| Series: | Frontiers in Zoology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12983-020-00364-y |
| _version_ | 1817989176390320128 |
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| author | Nicolás Cumplido Miguel L. Allende Gloria Arratia |
| author_facet | Nicolás Cumplido Miguel L. Allende Gloria Arratia |
| author_sort | Nicolás Cumplido |
| collection | DOAJ |
| description | Abstract Background With more than 30,000 species, teleosts comprise about half of today’s living vertebrates, enriched with a wide set of adaptations to all aquatic systems. Their evolution was marked by modifications of their tail, that involved major rearrangements of the metameric organization of the axial skeleton. The most posterior or ural caudal skeleton, primitively included more than 10 vertebrae and, through a series of fusions and losses, became reduced to a single vertebra in modern ostariophysans, one of the largest clades of teleosts. The ontogeny of the ostariophysan Danio rerio recapitulates this process by forming two or three separate vertebrae that become a single vertebra in adults. We characterize the developmental sequence of this change by describing the processes of patterning, fusion and differential growth on each of the constitutive elements that sculpt the adult terminal vertebra. Results The ontogenetic changes of the terminal vertebra were characterized, highlighting their shared and derived characters in comparison with other teleosts. In zebrafish, there is: i) a loss of the preural centrum 1, ii) the formation of an hourglass-shaped autocentrum only in the anterior but not the posterior border of the compound centrum, iii) the formation of a vestigial posterior centrum that does not form an autocentrum and becomes incorporated beneath the compound centrum during development, and iv) the elongated dorso-posterior process of the compound centrum or pleurostyle appears as an independent element posterior to the compound centrum, before fusing to the ural neural arches and the anterior portion of the compound centrum. Conclusions The unique features of the formation of the terminal vertebra in Danio rerio reflect the remarkable changes that occurred during the evolution of teleosts, with potential shared derived characteristics for some of the major lineages of modern teleosts. A new ontogenetic model is proposed to illustrate the development of the terminal vertebra, and the phylogenetic implications for the evolution of caudal skeleton consolidation in ostariophysans are discussed. |
| first_indexed | 2024-04-14T00:43:42Z |
| format | Article |
| id | doaj.art-e46835332fe34d908fb04b03238164e9 |
| institution | Directory Open Access Journal |
| issn | 1742-9994 |
| language | English |
| last_indexed | 2024-04-14T00:43:42Z |
| publishDate | 2020-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Frontiers in Zoology |
| spelling | doaj.art-e46835332fe34d908fb04b03238164e92022-12-22T02:22:07ZengBMCFrontiers in Zoology1742-99942020-06-0117111710.1186/s12983-020-00364-yFrom Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebraNicolás Cumplido0Miguel L. Allende1Gloria Arratia2FONDAP Center for Genome Regulation, Facultad de Ciencias, Universidad de ChileFONDAP Center for Genome Regulation, Facultad de Ciencias, Universidad de ChileUniversity of Kansas, Department of Ecology and Evolutionary Biology, Biodiversity InstituteAbstract Background With more than 30,000 species, teleosts comprise about half of today’s living vertebrates, enriched with a wide set of adaptations to all aquatic systems. Their evolution was marked by modifications of their tail, that involved major rearrangements of the metameric organization of the axial skeleton. The most posterior or ural caudal skeleton, primitively included more than 10 vertebrae and, through a series of fusions and losses, became reduced to a single vertebra in modern ostariophysans, one of the largest clades of teleosts. The ontogeny of the ostariophysan Danio rerio recapitulates this process by forming two or three separate vertebrae that become a single vertebra in adults. We characterize the developmental sequence of this change by describing the processes of patterning, fusion and differential growth on each of the constitutive elements that sculpt the adult terminal vertebra. Results The ontogenetic changes of the terminal vertebra were characterized, highlighting their shared and derived characters in comparison with other teleosts. In zebrafish, there is: i) a loss of the preural centrum 1, ii) the formation of an hourglass-shaped autocentrum only in the anterior but not the posterior border of the compound centrum, iii) the formation of a vestigial posterior centrum that does not form an autocentrum and becomes incorporated beneath the compound centrum during development, and iv) the elongated dorso-posterior process of the compound centrum or pleurostyle appears as an independent element posterior to the compound centrum, before fusing to the ural neural arches and the anterior portion of the compound centrum. Conclusions The unique features of the formation of the terminal vertebra in Danio rerio reflect the remarkable changes that occurred during the evolution of teleosts, with potential shared derived characteristics for some of the major lineages of modern teleosts. A new ontogenetic model is proposed to illustrate the development of the terminal vertebra, and the phylogenetic implications for the evolution of caudal skeleton consolidation in ostariophysans are discussed.http://link.springer.com/article/10.1186/s12983-020-00364-yEvo-DevoAxial skeletonUral regionPleurostyleCompound centrumAutocentrum |
| spellingShingle | Nicolás Cumplido Miguel L. Allende Gloria Arratia From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra Frontiers in Zoology Evo-Devo Axial skeleton Ural region Pleurostyle Compound centrum Autocentrum |
| title | From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra |
| title_full | From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra |
| title_fullStr | From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra |
| title_full_unstemmed | From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra |
| title_short | From Devo to Evo: patterning, fusion and evolution of the zebrafish terminal vertebra |
| title_sort | from devo to evo patterning fusion and evolution of the zebrafish terminal vertebra |
| topic | Evo-Devo Axial skeleton Ural region Pleurostyle Compound centrum Autocentrum |
| url | http://link.springer.com/article/10.1186/s12983-020-00364-y |
| work_keys_str_mv | AT nicolascumplido fromdevotoevopatterningfusionandevolutionofthezebrafishterminalvertebra AT miguellallende fromdevotoevopatterningfusionandevolutionofthezebrafishterminalvertebra AT gloriaarratia fromdevotoevopatterningfusionandevolutionofthezebrafishterminalvertebra |