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Origin of the Turtle Body Plan: The Folding Theory to Illustrate Turtle-Specific Developmental Repatterning

  • Hiroshi Nagashima
  • Shigehiro Kuraku
  • Katsuhisa Uchida
  • Yoshie Kawashima-Ohya
  • Yuichi Narita
  • Shigeru Kuratani
Chapter
Part of the Vertebrate Paleobiology and Paleoanthropology book series (VERT)

Abstract

The turtle shell is comprised of a dorsal carapace and a ventral plastron, and is an autapomorphy of this group. The carapace consists of the vertebral column and ribs as well as a specialized dermis. The formation of the shell is accompanied by a change in the spatial relationship of the ribs and the pectoral girdle. Because of this rearrangement, the turtle shell has been regarded as an example of an evolutionary novelty. Understanding the changes behind this developmental repatterning will help us elucidate the evolutionary history of turtles. The change has been attributed to a deflected pattern of development of the ribs, which in normal tetrapods grow ventrally into the lateral body wall. In turtles, they grow laterally toward the primordium of the carapacial margin, called the carapacial ridge (CR), while remaining in the axial part of the embryonic body. Based on a similarity in histological configuration, the CR has been thought to possess inductive activity for rib growth, as seen in the apical ectodermal ridge of the amniote limb bud. The CR does not function as a guidance cue for rib progenitor cells but rather functions in the marginal growth of the carapacial primordium, resulting in fanned-out growth of the ribs. This peripheral and concentric expansion of the axial domain makes the lateral body wall fold inward, while the ribs cover the pectoral girdle. The turtle ribs develop along the muscle plate as in other amniotes, and do not take a different trajectory from that in other amniotes, unlike the scenario hypothesized previously. This folding enables turtles to change the apparent spatial relationships between the ribs and the pectoral girdle without altering their topological alignment and body plan as amniotes. This developmental sequence of the modern turtles aligns with a stepwise evolutionary process in the group, which is supported by the anatomy of a recently discovered fossil species, Odontochelys.

Keywords

Carapacial ridge Development Odontochelys Proganochelys Ribs Turtle Shell 

Notes

Acknowledgments

We thank Dr. Don Brinkman for arranging the Gaffney Turtle Symposium and Festschrift publication in honor of Dr. Eugene S. Gaffney. We acknowledge Dr. Robert Carroll, Dr. Eugene S. Gaffney, and Dr. Olivier Rieppel for critical reading of the manuscript.

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Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Hiroshi Nagashima
    • 1
  • Shigehiro Kuraku
    • 1
  • Katsuhisa Uchida
    • 1
  • Yoshie Kawashima-Ohya
    • 1
  • Yuichi Narita
    • 1
  • Shigeru Kuratani
    • 1
  1. 1.Laboratory for Evolutionary MorphologyRIKEN Center for Developmental BiologyKobeJapan

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