Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution

TLDR

The turtle shell, a synapomorphic novelty in chelonians, originates when ribs are entrapped by the carapacial ridge, yet the mechanisms of rib entrapment, dorsal dermis ossification, and plastron formation remain unknown. We investigate plastron and carapace development in the red‑eared slider and snapping turtle through anatomical studies. Our studies show that ribs are entrapped by the carapacial ridge and that both carapace and plastron bones form via intramembranous ossification, with a complex nuchal ossification center comprising multiple bone‑forming regions. We found that each rib generates an ossification center that likely secretes paracrine factors to organize dermal ossification, that peripheral and pygial bones arise from distinct peripheral ossification centers, and that the plastron ossifies from nine interacting intramembranous centers.

Abstract

SUMMARY The turtle shell is an evolutionary novelty that is synapomorphic for chelonians. The carapace is initiated by the entrapment of the ribs by the carapacial ridge (CR), a lateral bulge of the dorsal ectoderm and dermal mesoderm. The mechanisms by which the CR is initiated, the ribs entrapped and the dorsal dermis ossified, remains unknown. Similarly, the formation of the plastron remains unexplained. Here, we present a series of anatomical investigations into plastron and carapace formation in the red‐eared slider, Trachemys scripta , and the snapping turtle, Chelydra serpentina. We document the entrapment of the ribs by the CR and the formation of the plastron and carapacial bones by intramembranous ossification. We note the formation of the ossification centers around each rib, which suggest that the rib is organizing dermal ossification by secreting paracrine factors. The nuchal ossification center is complex and appears to involve multiple bone‐forming regions. Individual ossification centers at the periphery of the carapace form the peripheral and pygial bones. The intramembranous ossification of the plastron proceeds from nine distinct ossification centers, and there appear to be interactions between the spicules of apposing centers as they draw near each other.