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. 2013:4:2107.
doi: 10.1038/ncomms3107.

The endoskeletal origin of the turtle carapace

Tatsuya Hirasawa  1 , Hiroshi Nagashima, Shigeru Kuratani
Affiliations
Free PMC article

The endoskeletal origin of the turtle carapace

Tatsuya Hirasawa et al. Nat Commun. 2013.
Free PMC article

Abstract

The turtle body plan, with its solid shell, deviates radically from those of other tetrapods. The dorsal part of the turtle shell, or the carapace, consists mainly of costal and neural bony plates, which are continuous with the underlying thoracic ribs and vertebrae, respectively. Because of their superficial position, the evolutionary origins of these costo-neural elements have long remained elusive. Here we show, through comparative morphological and embryological analyses, that the major part of the carapace is derived purely from endoskeletal ribs. We examine turtle embryos and find that the costal and neural plates develop not within the dermis, but within deeper connective tissue where the rib and intercostal muscle anlagen develop. We also examine the fossils of an outgroup of turtles to confirm that the structure equivalent to the turtle carapace developed independently of the true osteoderm. Our results highlight the hitherto unravelled evolutionary course of the turtle shell.

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Figures

Figure 1
Figure 1. Carapace of Chinese soft-shelled turtle Pelodiscus sinensis.
(a) Dorsal view. Scale bar, 1 cm. (b) Right half in ventral view. Red arrow indicates the costovertebral articulation. (c) Cleared and double-stained juvenile specimen. Scale bar, 5 mm. (d) Enlarged image of the immature costal plates in c. Box in c indicates the position of d. Scale bar, 2 mm. cos, costal plate; T1–T9, thoracic vertebra numbers; neu, neural plate; nu, nuchal.
Figure 2
Figure 2. Development of the costal plate in the turtle.
Hematoxylin-eosin-Alcian-blue-stained cross-sections of the ribs of the Chinese soft-shelled turtle (Pelodiscus sinensis). (a) Stage 17. Scale bar, 100 μm. (b) Stage 18. Scale bar, 100 μm. (c) Stage 21. Scale bar, 100 μm. (d) Stage 23. Scale bar, 100 μm. Arrows indicate direction of expansion of the periosteum (pos). (e) Stage 27. Scale bar, 100 μm. btr, bony trabecula; drm, dermis; epd, epidermis; icm, intercostal muscle; icn, intercostal nerve; ost, osteoblast; pob, periosteal bone collar; pos, periosteum; sdc, subdermal connective tissue.
Figure 3
Figure 3. Membranous bone formation of the rib in birds.
Hematoxylin-eosin-Alcian-blue-stained cross-section of the rib in a chicken (Gallus gallus) embryo at stage 40. (a) Delicate bony trabeculae (osteoids) at the insertion of the intercostal muscle (icm). Arrows indicate protrusion of bony trabeculae. Scale bar, 100 μm. (b) Bony trabeculae at the insertion of the intercostal muscle (icm). Scale bar, 100 μm. btr, bony trabecula; plc, pleural cavity; pob, periosteal bone collar; pos, periosteum; ost, osteoblast.
Figure 4
Figure 4. Middle Triassic marine reptile Sinosaurosphargis yunguiensis.
(a) Dorsal view of the holotype, IVPP V17040, preserving the skull and skeleton of the trunk region. Scale bar for the upper panels (a–c), 10 cm. (b) Ventral view of the paratype, IVPP V16076, preserving the skeleton of the trunk region. (c) Line drawing of b. (d) Enlarged image of the ribs and vertebrae in b. Box in b indicates the position of d. Scale bar, 1 cm. (e) Schematic structure of a transverse section of the rib cage in S. yunguiensis. (f) Phylogeny of the taxa examined. osd, osteoderm; ga, gastralia; tr, transverse process; vt, vertebra.
Figure 5
Figure 5. Evolution of the carapace by modification of the rib.
(a) Basal diapsids, possessing the movable rib cage. (b) Sinosaurosphargis (Middle Triassic). The laterally projected ribs were expanded to form the carapace, and the intercostal muscles were likely poorly developed. (c) Basal turtle species, Odontochelys (Late Triassic). The laterally projected ribs were expanded to form the carapace, and the intercostal muscles were likely poorly developed. (d) Modern turtles. The intercostal muscle anlage degenerates during embryonic development. Grey, integument; orange, epaxial muscles; red, hypaxial muscles including intercostal muscles.
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