Scott Gilbert/Judy Cebra-Thomas Lab

The development of the turtle carapace

Fraser Tan, Eileen Estes, Mike Cho, Christina Kim, Paul Riccio, Jacqui Simmonet, Brian Hwang, Katy Lewis

The turtle shell is the morphological innovation that defines the order Chelonia. The dorsal carapace consists of a series of bony plates surrounding each of the ribs and vertebrae, surrounded by a ring of peripheral bones and the large, trapezoidal nuccal bone above the neck. Although the carapace is composed of 50 unique bones, it appears abruptly in the fossil record, apparently without intermediates. At the same time, the body plan of chelonians has been highly modified; the ribs extend out laterally instead of wrapping ventrally to form a rib cage.At first glance, this appears to present a challenge to the conventionally accepted view that the evolution of novel structures should arise as a gradual progression. However, our investigations suggest that the carapacial bones form as a direct result of the alteration in the body plan. This results in the displacement of the ribs into the dermis and exposes the dermal cells to signaling molecules produced by the vertebrae and ribs. When the ribs undergo endochondral ossification, BMPs are produced that induce the surrounding and overlying dermis to become bone. This developmental sequence might explain the rapid emergence of turtles in the fossil record.

..The initiating event in carapace formation is the formation of a pair of thickened carapacial ridges in the dorsolateral ectoderm. These ridges and the underlying mesenchyme alter the migration of the somite derivatives. The sclerotome-derived rib precursors migrate laterally, out towards the carapacial ridges, and as a result the ribs end up positioned between the dermis and the myotome. Our data suggest that the key event, the formation of the carapacial ridges and the attraction of the rib precursors into them, is mediated by members of the fibroblast growth factor (FGF) family in the red eared slider Trachemys scripta. FGF10, which is expressed in the mesenchyme underlying the carapacial ridges, is a prime candidate for both maintenance of the ectodermal ridges and attraction of the sclerotome cells. FGF10 plays an important role in maintaining structures such as the limb apical ectodermal ridge and mammary bud placodes, and in addition has been shown to have chemattractant properties.

Treatment of chick embryo explants with beads containing FGF10 results in alterations in rib formation. In contrast, treatment of trunk explants in organ culture with a specific inhibitor of FGF signaling (SU5402) blocks the maintenance of the carapacial ridges and the allows the somite derivates to develop in a manner similar to other vertebrates.

The outgrowth and patterning of structures such as limbs and feathers is the result of coordinated signaling by FGFs, Wnts and sonic hedgehog (SHH). We have recently demonstrated that early crapacial ridge ectoderm (stage15) expresses sonic hedgehog (shh) and contains nuclear b-catenin (a marker of Wnt signaling), suggesting that a similar integration of FGF, Wnt and SHH signals may be important in carapacial ridge outgrowth.

@Cebra-Thomas, 2006

Last Modified: 24 January 2006

[ Cebra-Thomas ]

	The turtle shell is the morphological innovation that defines the order Chelonia. The dorsal carapace consists of a series of bony plates surrounding each of the ribs and vertebrae, surrounded by a ring of peripheral bones and the large, trapezoidal nuccal bone above the neck. Although the carapace is composed of 50 unique bones, it appears abruptly in the fossil record, apparently without intermediates. At the same time, the body plan of chelonians has been highly modified; the ribs extend out laterally instead of wrapping ventrally to form a rib cage.At first glance, this appears to present a challenge to the conventionally accepted view that the evolution of novel structures should arise as a gradual progression. However, our investigations suggest that the carapacial bones form as a direct result of the alteration in the body plan. This results in the displacement of the ribs into the dermis and exposes the dermal cells to signaling molecules produced by the vertebrae and ribs. When the ribs undergo endochondral ossification, BMPs are produced that induce the surrounding and overlying dermis to become bone. This developmental sequence might explain the rapid emergence of turtles in the fossil record.
..The initiating event in carapace formation is the formation of a pair of thickened carapacial ridges in the dorsolateral ectoderm. These ridges and the underlying mesenchyme alter the migration of the somite derivatives. The sclerotome-derived rib precursors migrate laterally, out towards the carapacial ridges, and as a result the ribs end up positioned between the dermis and the myotome. Our data suggest that the key event, the formation of the carapacial ridges and the attraction of the rib precursors into them, is mediated by members of the fibroblast growth factor (FGF) family in the red eared slider Trachemys scripta. FGF10, which is expressed in the mesenchyme underlying the carapacial ridges, is a prime candidate for both maintenance of the ectodermal ridges and attraction of the sclerotome cells. FGF10 plays an important role in maintaining structures such as the limb apical ectodermal ridge and mammary bud placodes, and in addition has been shown to have chemattractant properties.
	Treatment of chick embryo explants with beads containing FGF10 results in alterations in rib formation. In contrast, treatment of trunk explants in organ culture with a specific inhibitor of FGF signaling (SU5402) blocks the maintenance of the carapacial ridges and the allows the somite derivates to develop in a manner similar to other vertebrates.
The outgrowth and patterning of structures such as limbs and feathers is the result of coordinated signaling by FGFs, Wnts and sonic hedgehog (SHH). We have recently demonstrated that early crapacial ridge ectoderm (stage15) expresses sonic hedgehog (shh) and contains nuclear b-catenin (a marker of Wnt signaling), suggesting that a similar integration of FGF, Wnt and SHH signals may be important in carapacial ridge outgrowth.