New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.

From early dinosaurs with as many as nine wrist bones, modern birds evolved to develop only four ossifications. Their identity is uncertain, with different labels used in palaeontology and developmental biology. We examined embryos of several species and studied chicken embryos in detail through a n...

Full description

Bibliographic Details
Main Authors: João Francisco Botelho, Luis Ossa-Fuentes, Sergio Soto-Acuña, Daniel Smith-Paredes, Daniel Nuñez-León, Miguel Salinas-Saavedra, Macarena Ruiz-Flores, Alexander O Vargas
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-09-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC4181957?pdf=render
_version_ 1818883994028081152
author João Francisco Botelho
Luis Ossa-Fuentes
Sergio Soto-Acuña
Daniel Smith-Paredes
Daniel Nuñez-León
Miguel Salinas-Saavedra
Macarena Ruiz-Flores
Alexander O Vargas
author_facet João Francisco Botelho
Luis Ossa-Fuentes
Sergio Soto-Acuña
Daniel Smith-Paredes
Daniel Nuñez-León
Miguel Salinas-Saavedra
Macarena Ruiz-Flores
Alexander O Vargas
author_sort João Francisco Botelho
collection DOAJ
description From early dinosaurs with as many as nine wrist bones, modern birds evolved to develop only four ossifications. Their identity is uncertain, with different labels used in palaeontology and developmental biology. We examined embryos of several species and studied chicken embryos in detail through a new technique allowing whole-mount immunofluorescence of the embryonic cartilaginous skeleton. Beyond previous controversy, we establish that the proximal-anterior ossification develops from a composite radiale+intermedium cartilage, consistent with fusion of radiale and intermedium observed in some theropod dinosaurs. Despite previous claims that the development of the distal-anterior ossification does not support the dinosaur-bird link, we found its embryonic precursor shows two distinct regions of both collagen type II and collagen type IX expression, resembling the composite semilunate bone of bird-like dinosaurs (distal carpal 1+distal carpal 2). The distal-posterior ossification develops from a cartilage referred to as "element x," but its position corresponds to distal carpal 3. The proximal-posterior ossification is perhaps most controversial: It is labelled as the ulnare in palaeontology, but we confirm the embryonic ulnare is lost during development. Re-examination of the fossil evidence reveals the ulnare was actually absent in bird-like dinosaurs. We confirm the proximal-posterior bone is a pisiform in terms of embryonic position and its development as a sesamoid associated to a tendon. However, the pisiform is absent in bird-like dinosaurs, which are known from several articulated specimens. The combined data provide compelling evidence of a remarkable evolutionary reversal: A large, ossified pisiform re-evolved in the lineage leading to birds, after a period in which it was either absent, nonossified, or very small, consistently escaping fossil preservation. The bird wrist provides a modern example of how developmental and paleontological data illuminate each other. Based on all available data, we introduce a new nomenclature for bird wrist ossifications.
first_indexed 2024-12-19T15:42:29Z
format Article
id doaj.art-9a867d0522d544ceaf0b18c59b3c1182
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-12-19T15:42:29Z
publishDate 2014-09-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-9a867d0522d544ceaf0b18c59b3c11822022-12-21T20:15:26ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-09-01129e100195710.1371/journal.pbio.1001957New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.João Francisco BotelhoLuis Ossa-FuentesSergio Soto-AcuñaDaniel Smith-ParedesDaniel Nuñez-LeónMiguel Salinas-SaavedraMacarena Ruiz-FloresAlexander O VargasFrom early dinosaurs with as many as nine wrist bones, modern birds evolved to develop only four ossifications. Their identity is uncertain, with different labels used in palaeontology and developmental biology. We examined embryos of several species and studied chicken embryos in detail through a new technique allowing whole-mount immunofluorescence of the embryonic cartilaginous skeleton. Beyond previous controversy, we establish that the proximal-anterior ossification develops from a composite radiale+intermedium cartilage, consistent with fusion of radiale and intermedium observed in some theropod dinosaurs. Despite previous claims that the development of the distal-anterior ossification does not support the dinosaur-bird link, we found its embryonic precursor shows two distinct regions of both collagen type II and collagen type IX expression, resembling the composite semilunate bone of bird-like dinosaurs (distal carpal 1+distal carpal 2). The distal-posterior ossification develops from a cartilage referred to as "element x," but its position corresponds to distal carpal 3. The proximal-posterior ossification is perhaps most controversial: It is labelled as the ulnare in palaeontology, but we confirm the embryonic ulnare is lost during development. Re-examination of the fossil evidence reveals the ulnare was actually absent in bird-like dinosaurs. We confirm the proximal-posterior bone is a pisiform in terms of embryonic position and its development as a sesamoid associated to a tendon. However, the pisiform is absent in bird-like dinosaurs, which are known from several articulated specimens. The combined data provide compelling evidence of a remarkable evolutionary reversal: A large, ossified pisiform re-evolved in the lineage leading to birds, after a period in which it was either absent, nonossified, or very small, consistently escaping fossil preservation. The bird wrist provides a modern example of how developmental and paleontological data illuminate each other. Based on all available data, we introduce a new nomenclature for bird wrist ossifications.http://europepmc.org/articles/PMC4181957?pdf=render
spellingShingle João Francisco Botelho
Luis Ossa-Fuentes
Sergio Soto-Acuña
Daniel Smith-Paredes
Daniel Nuñez-León
Miguel Salinas-Saavedra
Macarena Ruiz-Flores
Alexander O Vargas
New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
PLoS Biology
title New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
title_full New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
title_fullStr New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
title_full_unstemmed New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
title_short New developmental evidence clarifies the evolution of wrist bones in the dinosaur-bird transition.
title_sort new developmental evidence clarifies the evolution of wrist bones in the dinosaur bird transition
url http://europepmc.org/articles/PMC4181957?pdf=render
work_keys_str_mv AT joaofranciscobotelho newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT luisossafuentes newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT sergiosotoacuna newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT danielsmithparedes newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT danielnunezleon newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT miguelsalinassaavedra newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT macarenaruizflores newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition
AT alexanderovargas newdevelopmentalevidenceclarifiestheevolutionofwristbonesinthedinosaurbirdtransition