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

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Morphology and Evolution of Turtles

Part of the book series: Vertebrate Paleobiology and Paleoanthropology ((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.

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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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Author notes

  1. Hiroshi Nagashima

    Present address: Division of Gross Anatomy and Morphogenesis, Department of Regenerative and Transplant Medicine, Niigata University, Niigata, 951-8510, Japan

  2. Shigehiro Kuraku

    Present address: Genome Resource and Analysis Unit, RIKEN Center for Developmental Biology, Kobe, 650-0047, Japan

  3. Katsuhisa Uchida

    Present address: Department of Marine Biology and Environmental Sciences, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuen Kibanadai-nishi, Miyazaki, 889-2192, Japan

  4. Yoshie Kawashima-Ohya

    Present address: Laboratory of Immunology, Department of Health Pharmacy, Yokohama College of Pharmacy, 601 Matano-cho, Totsuka-ku, Yokohama, 245-0066, Japan

  5. Yuichi Narita

    Present address: Department of Food Business, Faculty of Health and Human Life, Nagoya Bunri University, 365 Maeda, Inazawa-cho, Inazawa, 492-8520, Japan

Authors and Affiliations

  1. Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, Kobe, 650-0047, Japan

    Hiroshi Nagashima, Shigehiro Kuraku, Katsuhisa Uchida, Yoshie Kawashima-Ohya, Yuichi Narita & Shigeru Kuratani

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  1. Hiroshi Nagashima
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Correspondence to Shigeru Kuratani .

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  1. Royal Tyrell Museum, Drumheller, Alberta, Canada

    Donald B. Brinkman

  2. Museum of Paleontology, University of California, Berkeley, California, USA

    Patricia A. Holroyd

  3. Royal Tyrrell Museum, Drumheller, Canada

    James D. Gardner

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Nagashima, H., Kuraku, S., Uchida, K., Kawashima-Ohya, Y., Narita, Y., Kuratani, S. (2013). Origin of the Turtle Body Plan: The Folding Theory to Illustrate Turtle-Specific Developmental Repatterning. In: Brinkman, D., Holroyd, P., Gardner, J. (eds) Morphology and Evolution of Turtles. Vertebrate Paleobiology and Paleoanthropology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4309-0_4

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