title: The origin and loss of periodic patterning in the turtle shell.
abstract: The origin of the turtle shell over 200 million years ago greatly modified the amniote body plan, and the morphological plasticity of the shell has promoted the adaptive radiation of turtles. The shell, comprising a dorsal carapace and a ventral plastron, is a layered structure formed by basal endochondral axial skeletal elements (ribs, vertebrae) and plates of bone, which are overlain by keratinous ectodermal scutes. Studies of turtle development have mostly focused on the bones of the shell; however, the genetic regulation of the epidermal scutes has not been investigated. Here, we show that scutes develop from an array of patterned placodes and that these placodes are absent from a soft-shelled turtle in which scutes were lost secondarily. Experimentally inhibiting Shh, Bmp or Fgf signaling results in the disruption of the placodal pattern. Finally, a computational model is used to show how two coupled reaction-diffusion systems reproduce both natural and abnormal variation in turtle scutes. Taken together, these placodal signaling centers are likely to represent developmental modules that are responsible for the evolution of scutes in turtles, and the regulation of these centers has allowed for the diversification of the turtle shell.
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland jacqueline.moustakas@helsinki.fi sgilber1@swarthmore.edu.
authors: Jacqueline E
authors: JE
authors: Moustakas-Verho
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland.
authors: Roland
authors: R
authors: Zimm
authors: Biology Department, Millersville University, P.O. Box 1002, Millersville, PA 17551, USA.
authors: Judith
authors: J
authors: Cebra-Thomas
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland.
authors: Netta K
authors: NK
authors: Lempiäinen
authors: Division of Materials Physics, Department of Physics, University of Helsinki, P.O. Box 64, Helsinki FIN-00014, Finland.
authors: Aki
authors: A
authors: Kallonen
authors: Biology Department, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081, USA.
authors: Katherine L
authors: KL
authors: Mitchell
authors: Division of Materials Physics, Department of Physics, University of Helsinki, P.O. Box 64, Helsinki FIN-00014, Finland.
authors: Keijo
authors: K
authors: Hämäläinen
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Barcelona, Spain.
authors: Isaac
authors: I
authors: Salazar-Ciudad
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland.
authors: Jukka
authors: J
authors: Jernvall
authors: Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland Biology Department, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081, USA jacqueline.moustakas@helsinki.fi sgilber1@swarthmore.edu.
authors: Scott F
authors: SF
authors: Gilbert
mesh_terms: D060105:Animal Shells / Q000196:embryology* / Q000502:physiology; D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning; D001846:Bone Development; D019485:Bone Morphogenetic Proteins / Q000378:metabolism; D003198:Computer Simulation; D004625:Embryo, Nonmammalian / Q000033:anatomy & histology; D005346:Fibroblast Growth Factors / Q000378:metabolism; D005786:Gene Expression Regulation; D053823:Hedgehog Proteins / Q000378:metabolism; D021621:Imaging, Three-Dimensional; D017403:In Situ Hybridization; D015398:Signal Transduction; D014426:Turtles / Q000196:embryology* / Q000502:physiology
chemical_list: D019485:Bone Morphogenetic Proteins; D053823:Hedgehog Proteins; D005346:Fibroblast Growth Factors
keywords: Ectodermal appendage; Placode; Scute; Shh; Turtle