Cargando…
Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty
Developmental novelties often underlie the evolutionary origins of key metazoan features. The anuran urostyle, which evolved nearly 200 MYA, is one such structure. It forms as the tail regresses during metamorphosis, when locomotion changes from an axial-driven mode in larvae to a limb-driven one in...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022158/ https://www.ncbi.nlm.nih.gov/pubmed/31988131 http://dx.doi.org/10.1073/pnas.1917506117 |
_version_ | 1783497968819634176 |
---|---|
author | Senevirathne, Gayani Baumgart, Stephanie Shubin, Nathaniel Hanken, James Shubin, Neil H. |
author_facet | Senevirathne, Gayani Baumgart, Stephanie Shubin, Nathaniel Hanken, James Shubin, Neil H. |
author_sort | Senevirathne, Gayani |
collection | PubMed |
description | Developmental novelties often underlie the evolutionary origins of key metazoan features. The anuran urostyle, which evolved nearly 200 MYA, is one such structure. It forms as the tail regresses during metamorphosis, when locomotion changes from an axial-driven mode in larvae to a limb-driven one in adult frogs. The urostyle comprises of a coccyx and a hypochord. The coccyx forms by fusion of caudal vertebrae and has evolved repeatedly across vertebrates. However, the contribution of an ossifying hypochord to the coccyx in anurans is unique among vertebrates and remains a developmental enigma. Here, we focus on the developmental changes that lead to the anuran urostyle, with an emphasis on understanding the ossifying hypochord. We find that the coccyx and hypochord have two different developmental histories: First, the development of the coccyx initiates before metamorphic climax whereas the ossifying hypochord undergoes rapid ossification and hypertrophy; second, thyroid hormone directly affects hypochord formation and appears to have a secondary effect on the coccygeal portion of the urostyle. The embryonic hypochord is known to play a significant role in the positioning of the dorsal aorta (DA), but the reason for hypochordal ossification remains obscure. Our results suggest that the ossifying hypochord plays a role in remodeling the DA in the newly forming adult body by partially occluding the DA in the tail. We propose that the ossifying hypochord-induced loss of the tail during metamorphosis has enabled the evolution of the unique anuran bauplan. |
format | Online Article Text |
id | pubmed-7022158 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-70221582020-02-21 Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty Senevirathne, Gayani Baumgart, Stephanie Shubin, Nathaniel Hanken, James Shubin, Neil H. Proc Natl Acad Sci U S A Biological Sciences Developmental novelties often underlie the evolutionary origins of key metazoan features. The anuran urostyle, which evolved nearly 200 MYA, is one such structure. It forms as the tail regresses during metamorphosis, when locomotion changes from an axial-driven mode in larvae to a limb-driven one in adult frogs. The urostyle comprises of a coccyx and a hypochord. The coccyx forms by fusion of caudal vertebrae and has evolved repeatedly across vertebrates. However, the contribution of an ossifying hypochord to the coccyx in anurans is unique among vertebrates and remains a developmental enigma. Here, we focus on the developmental changes that lead to the anuran urostyle, with an emphasis on understanding the ossifying hypochord. We find that the coccyx and hypochord have two different developmental histories: First, the development of the coccyx initiates before metamorphic climax whereas the ossifying hypochord undergoes rapid ossification and hypertrophy; second, thyroid hormone directly affects hypochord formation and appears to have a secondary effect on the coccygeal portion of the urostyle. The embryonic hypochord is known to play a significant role in the positioning of the dorsal aorta (DA), but the reason for hypochordal ossification remains obscure. Our results suggest that the ossifying hypochord plays a role in remodeling the DA in the newly forming adult body by partially occluding the DA in the tail. We propose that the ossifying hypochord-induced loss of the tail during metamorphosis has enabled the evolution of the unique anuran bauplan. National Academy of Sciences 2020-02-11 2020-01-27 /pmc/articles/PMC7022158/ /pubmed/31988131 http://dx.doi.org/10.1073/pnas.1917506117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Senevirathne, Gayani Baumgart, Stephanie Shubin, Nathaniel Hanken, James Shubin, Neil H. Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title | Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title_full | Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title_fullStr | Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title_full_unstemmed | Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title_short | Ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
title_sort | ontogeny of the anuran urostyle and the developmental context of evolutionary novelty |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022158/ https://www.ncbi.nlm.nih.gov/pubmed/31988131 http://dx.doi.org/10.1073/pnas.1917506117 |
work_keys_str_mv | AT senevirathnegayani ontogenyoftheanuranurostyleandthedevelopmentalcontextofevolutionarynovelty AT baumgartstephanie ontogenyoftheanuranurostyleandthedevelopmentalcontextofevolutionarynovelty AT shubinnathaniel ontogenyoftheanuranurostyleandthedevelopmentalcontextofevolutionarynovelty AT hankenjames ontogenyoftheanuranurostyleandthedevelopmentalcontextofevolutionarynovelty AT shubinneilh ontogenyoftheanuranurostyleandthedevelopmentalcontextofevolutionarynovelty |