Forelimb-hindlimb developmental timing changes across tetrapod phylogeny

<p>Abstract</p> <p>Background</p> <p>Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential...

Full description

Bibliographic Details
Main Authors: Selwood Lynne, Pieau Claude, Colbert Matthew, Hanken James, Sánchez-Villagra Marcelo R, Jeffery Jonathan E, Bininda-Emonds Olaf RP, ten Cate Carel, Raynaud Albert, Osabutey Casmile K, Richardson Michael K
Format: Article
Language:English
Published: BMC 2007-10-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/7/182
id doaj-0a102dcdd35a47abbc07d3a70f09bab0
record_format Article
spelling doaj-0a102dcdd35a47abbc07d3a70f09bab02021-09-02T06:22:26ZengBMCBMC Evolutionary Biology1471-21482007-10-017118210.1186/1471-2148-7-182Forelimb-hindlimb developmental timing changes across tetrapod phylogenySelwood LynnePieau ClaudeColbert MatthewHanken JamesSánchez-Villagra Marcelo RJeffery Jonathan EBininda-Emonds Olaf RPten Cate CarelRaynaud AlbertOsabutey Casmile KRichardson Michael K<p>Abstract</p> <p>Background</p> <p>Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.</p> <p>Results</p> <p>An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.</p> <p>Conclusion</p> <p>Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.</p> http://www.biomedcentral.com/1471-2148/7/182
collection DOAJ
language English
format Article
sources DOAJ
author Selwood Lynne
Pieau Claude
Colbert Matthew
Hanken James
Sánchez-Villagra Marcelo R
Jeffery Jonathan E
Bininda-Emonds Olaf RP
ten Cate Carel
Raynaud Albert
Osabutey Casmile K
Richardson Michael K
spellingShingle Selwood Lynne
Pieau Claude
Colbert Matthew
Hanken James
Sánchez-Villagra Marcelo R
Jeffery Jonathan E
Bininda-Emonds Olaf RP
ten Cate Carel
Raynaud Albert
Osabutey Casmile K
Richardson Michael K
Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
BMC Evolutionary Biology
author_facet Selwood Lynne
Pieau Claude
Colbert Matthew
Hanken James
Sánchez-Villagra Marcelo R
Jeffery Jonathan E
Bininda-Emonds Olaf RP
ten Cate Carel
Raynaud Albert
Osabutey Casmile K
Richardson Michael K
author_sort Selwood Lynne
title Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
title_short Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
title_full Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
title_fullStr Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
title_full_unstemmed Forelimb-hindlimb developmental timing changes across tetrapod phylogeny
title_sort forelimb-hindlimb developmental timing changes across tetrapod phylogeny
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2007-10-01
description <p>Abstract</p> <p>Background</p> <p>Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.</p> <p>Results</p> <p>An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.</p> <p>Conclusion</p> <p>Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.</p>
url http://www.biomedcentral.com/1471-2148/7/182
work_keys_str_mv AT selwoodlynne forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT pieauclaude forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT colbertmatthew forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT hankenjames forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT sanchezvillagramarcelor forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT jefferyjonathane forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT binindaemondsolafrp forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT tencatecarel forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT raynaudalbert forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT osabuteycasmilek forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
AT richardsonmichaelk forelimbhindlimbdevelopmentaltimingchangesacrosstetrapodphylogeny
_version_ 1721179029107638272