title: Molecular development of fibular reduction in birds and its evolution from dinosaurs.
abstract: Birds have a distally reduced, splinter-like fibula that is shorter than the tibia. In embryonic development, both skeletal elements start out with similar lengths. We examined molecular markers of cartilage differentiation in chicken embryos. We found that the distal end of the fibula expresses Indian hedgehog (IHH), undergoing terminal cartilage differentiation, and almost no Parathyroid-related protein (PTHrP), which is required to develop a proliferative growth plate (epiphysis). Reduction of the distal fibula may be influenced earlier by its close contact with the nearby fibulare, which strongly expresses PTHrP. The epiphysis-like fibulare however then separates from the fibula, which fails to maintain a distal growth plate, and fibular reduction ensues. Experimental downregulation of IHH signaling at a postmorphogenetic stage led to a tibia and fibula of equal length: The fibula is longer than in controls and fused to the fibulare, whereas the tibia is shorter and bent. We propose that the presence of a distal fibular epiphysis may constrain greater growth in the tibia. Accordingly, many Mesozoic birds show a fibula that has lost its distal epiphysis, but remains almost as long as the tibia, suggesting that loss of the fibulare preceded and allowed subsequent evolution of great fibulo-tibial disparity.
authors.affiliation: Laboratorio de Ontogenia y Filogenia, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile. joaofranciscobotelho@gmail.com.
authors.forename: João Francisco
authors.initials: JF
authors.lastname: Botelho
authors.affiliation: Laboratorio de Ontogenia y Filogenia, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile.
authors.forename: Daniel
authors.initials: D
authors.lastname: Smith-Paredes
authors.affiliation: Laboratorio de Ontogenia y Filogenia, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile.|Área de Paleontología, Museo Nacional de Historia Natural, Santiago, Chile.
authors.forename: Sergio
authors.initials: S
authors.lastname: Soto-Acuña
authors.affiliation: Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Science, Beijing, China.
authors.forename: Jingmai
authors.initials: J
authors.lastname: O'Connor
authors.affiliation: FONDAP Center for Genomic Regulation, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile.
authors.forename: Verónica
authors.initials: V
authors.lastname: Palma
authors.affiliation: Laboratorio de Ontogenia y Filogenia, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile. alexvargas@uchile.cl.
authors.forename: Alexander O
authors.initials: AO
authors.lastname: Vargas
mesh_terms: D000818:Animals; D030161:Avian Proteins / Q000235:genetics / Q000378:metabolism; D005075:Biological Evolution; D001717:Birds / Q000033:anatomy & histology* / Q000145:classification / Q000196:embryology / Q000235:genetics*; D002356:Cartilage / Q000378:metabolism; D025061:Dinosaurs / Q000033:anatomy & histology; D005360:Fibula / Q000033:anatomy & histology* / Q000196:embryology / Q000502:physiology; D005580:Fossils / Q000033:anatomy & histology; D006132:Growth Plate / Q000378:metabolism; D053823:Hedgehog Proteins / Q000378:metabolism; D010012:Osteogenesis
chemical_list: D030161:Avian Proteins; D053823:Hedgehog Proteins
keywords: Bird-dinosaur transition; PTHrP; fibula, IHH; mesozoic birds; zeugopod