Research article

Forelimb-hindlimb developmental timing changes across tetrapod phylogeny

Olaf RP Bininda-Emonds^{* 1,2} , Jonathan E Jeffery^{* 1} , Marcelo R Sánchez-Villagra^{* 3} , James Hanken⁴ , Matthew Colbert⁵ , Claude Pieau⁶ , Lynne Selwood⁷ , Carel ten Cate¹ , Albert Raynaud^{^ 8}, Casmile K Osabutey⁹ and Michael K Richardson¹

¹Institute of Biology, University of Leiden, Kaiserstraat 63, 2311GP, Leiden, The Netherlands

²Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstrasse 1, 07743 Jena, Germany

³Palaeontologisches Institut und Museum, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland

⁴Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

⁵Department of Geological Sciences, The University of Texas, Austin, TX 78712, USA

⁶Laboratoire de Biochimie du Développement, Institut Jacques Monod, CNRS et Université Paris 6 et 7, Tour 43-33, E3, 2, place Jussieu, 75251 Paris Cedex 05, France

⁷Department of Zoology, Gate 12, University of Melbourne, Victoria. 3010, Australia

⁸Formerly of Laboratoire Pasteur (Embryologie expérimentale), 20 rue des Moulins, 95110 Sannois, France

⁹Department of Anatomy, St George's Hospital Medical School, Tooting, London SW17 0RE, UK

author email corresponding author email^Deceased * Contributed equally

BMC Evolutionary Biology 2007, 7:182doi:10.1186/1471-2148-7-182

Published:	1 October 2007

Abstract

Background

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.

Results

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.

Conclusion

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.