Development of the turtle plastron, the order-defining skeletal structure

Abstract

The dorsal and ventral aspects of the turtle shell, the carapace and the plastron, are developmentally different entities. The carapace contains axial endochondral skeletal elements and exoskeletal dermal bones. The exoskeletal plastron is found in all extant and extinct species of crown turtles found to date and is synaptomorphic of the order Testudines. However, paleontological reconstructed transition forms lack a fully developed carapace and show a progression of bony elements ancestral to the plastron. To understand the evolutionary development of the plastron, it is essential to know how it has formed. Here we studied the molecular development and patterning of plastron bones in a cryptodire turtle Trachemys scripta. We show that plastron development begins at developmental stage 15 when osteochondrogenic mesenchyme forms condensates for each plastron bone at the lateral edges of the ventral mesenchyme. These condensations commit to an osteogenic identity and suppress chondrogenesis. Their development overlaps with that of sternal cartilage development in chicks and mice. Thus, we suggest that in turtles, the sternal morphogenesis is prevented in the ventral mesenchyme by the concomitant induction of osteogenesis and the suppression of chondrogenesis. The osteogenic subroutines later direct the growth and patterning of plastron bones in an autonomous manner. The initiation of plastron bone development coincides with that of carapacial ridge formation, suggesting that the development of dorsal and ventral shells are coordinated from the start and that adopting an osteogenesis-inducing and chondrogenesissuppressing cell fate in the ventral mesenchyme has permitted turtles to develop their order-specific ventral morphology.turtle | plastron | osteogenesis | development

The origin of the turtle body plan: evidence from fossils and embryos

“…Rice et al . () demonstrated that the relative position and timing of the plastral condensations indeed matches those of the precursors of the sternal cartilages in birds and mice. However, the condensations in the ventral mesenchyme of turtle embryos commit to bone formation and hence suppress the development of sternal cartilages.…”

“…It is interesting to note that ossification of the carapace lags behind that of the plastron in extant turtles (Rieppel ) even though the onset of the ontogenetic development of both halves of the turtle shell coincides (Rice et al . ). Clark et al .…”

Beauty is more than skin deep: a non‐invasive protocol for in vivo anatomical study using micro‐CT

“…In the second example, researchers might want to provide more insight into the development of the carapace in the Angulate tortoise, Chersina angulate (e.g. Rice et al 2016).…”

Patterns of morphological evolution in the skull of turtles: contributions from digital paleontology, neuroanatomy and biomechanics

“…Even though a less detailed scenario is currently known for the morphological and developmental origins of the plastron, recent research presented important advancements (Cherepanov 1997;Cebra-Thomas et al 2007Rice et al 2016). Most extant turtles possess nine bones in the plastron (Zangerl 1969), but stem-turtles, e.g.…”

“…From those, the three anterior plates, the epiplastra and entoplastron, are thought to be derived from the clavicles and interclavicles, respectively (Cherepanov 1997;Lyson et al 2013) and the posterior plates have been associated with modified paired abdominal ribs, the gastralia (Romer 1956;Gaffney 1990;Kuratani et al 2011), even though a distinct type of ossification (forming bone spicules) is characteristic of plastral bones (Rice et al 2016). It has been shown that those plates have an important contribution from neural crest cells (Cebra-Thomas et al 2007Gilbert et al 2007) and that their appearance suppresses the development of a sternum in the ventral part of the embryonic turtle body and is concomitant with that of the carapacial ridge (Rice et al 2016). Thus, albeit more work needs to be done to better understand the nature of the plastron, its appearance also seems to be related to the evolutionary novelty of turtles, the carapacial ridge (Kuratani et al 2011).…”