title: Forelimb-hindlimb developmental timing changes across tetrapod phylogeny.
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.
  
  
  CONCLUSIONS
  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.
authors.affiliation: Institute of Biology, University of Leiden, Kaiserstraat 63, 2311GP, Leiden, The Netherlands. Olaf.Bininda@uni-jena.de
authors.forename: Olaf R P
authors.initials: OR
authors.lastname: Bininda-Emonds
authors.forename: Jonathan E
authors.initials: JE
authors.lastname: Jeffery
authors.forename: Marcelo R
authors.initials: MR
authors.lastname: Sánchez-Villagra
authors.forename: James
authors.initials: J
authors.lastname: Hanken
authors.forename: Matthew
authors.initials: M
authors.lastname: Colbert
authors.forename: Claude
authors.initials: C
authors.lastname: Pieau
authors.forename: Lynne
authors.initials: L
authors.lastname: Selwood
authors.forename: Carel
authors.initials: C
authors.lastname: Ten Cate
authors.forename: Albert
authors.initials: A
authors.lastname: Raynaud
authors.forename: Casmile K
authors.initials: CK
authors.lastname: Osabutey
authors.forename: Michael K
authors.initials: MK
authors.lastname: Richardson
mesh_terms: D000818:Animals; D001001:Anura / Q000254:growth & development; D001717:Birds / Q000254:growth & development; D004622:Embryo, Mammalian; D004625:Embryo, Nonmammalian; D007312:Eulipotyphla / Q000254:growth & development; D005552:Forelimb / Q000196:embryology / Q000254:growth & development*; D006614:Hindlimb / Q000196:embryology / Q000254:growth & development*; D018878:Limb Buds / Q000254:growth & development; D008116:Lizards / Q000254:growth & development; D051379:Mice; D010802:Phylogeny; D013045:Species Specificity; D014714:Vertebrates / Q000254:growth & development*