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...

Descripción completa

Detalles Bibliográficos
Autores principales: Senevirathne, Gayani, Baumgart, Stephanie, Shubin, Nathaniel, Hanken, James, Shubin, Neil H.
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