Evidence that a late‐emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta

Abstract

The origin of the turtle plastron is not known, but these nine bones have been homologized to the exoskeletal components of the clavicles, the interclavicular bone, and gastralia. Earlier evidence from our laboratory showed that the bone-forming cells of the plastron were positive for HNK-1 and PDGFRalpha, two markers of the skeletogenic neural crest. This study looks at the embryonic origin of these plastron-forming cells. We show that the HNK-1+ cells are also positive for p75 and FoxD3, confirming their neural crest identity, and that they originate from the dorsal neural tube of stage 17 turtle embryos, several days after the original wave of neural crest cells have migrated and differentiated. DiI studies show that these are migratory cells, and they can be observed in the lateral regions of the embryo and can be seen forming intramembranous bone in the ventral (plastron) regions. Before migrating ventrally, these late-emerging neural crest cells reside for over a week in a carapacial staging area above the neural tube and vertebrae. It is speculated that this staging area is where they lose the inability to form skeletal cells.

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

“…Several recent studies have shown turtles to be the sister group to the archosaurs (47-51), and a possible ancestral lineage has been proposed (45). The turtle plastron, its possible origin (52,53) and homologies (6,45) to skeletal elements found in other tetrapods have been studied and discussed for decades, yet this is the first study to our knowledge that has established a developmental timeline and location for plastron bone development from their early uncommitted mesenchymal condensations to the development and growth of bone extensions. This study also investigates the patterning information used in plastron bone growth.…”

Review: The Role of Neural Crest Cells in the Endocrine System

“…Smith and Hall have also found evidence that some groups of fossil fish (such as placoderms, a prehistoric class of armored, jawed fish) and some extant fish with dermal denticles on the postcranial skeleton or some fin rays (including the dermal rays in the caudal fin of zebrafish) may also have osteogenic trunk neural crest cells [22,[24][25][26][27]. There is some evidence that the gastralia (paired dermal "abdominal ribs" seen in some extant reptiles) might be derived from trunk neural crest cells as well [22]. Trunk crest can be odontogenic as shown when the most rostral axolotl trunk neural crest is combined with endoderm (inducer of teeth in the axolotl) [28].…”

“…In addition to the C cells of the thyroid, the cranial neural crest cells are those that emerge from the presumptive brain region to form many of the craniofacial cartilages and bones as well as nerves and connective tissues. The skeletogenic potential of the cranial neural crest has been widely explored and documented throughout the Vertebrata subphylum, though trunk neural crest cells can also contribute to skeletal elements in some animals such as the plastron bones of the red-eared slider turtle (Trachemys scripta) and some trunk crest retain potential to form bone and cartilage in other amniotes as well [21][22][23], though this is fairly limited. Smith and Hall have also found evidence that some groups of fossil fish (such as placoderms, a prehistoric class of armored, jawed fish) and some extant fish with dermal denticles on the postcranial skeleton or some fin rays (including the dermal rays in the caudal fin of zebrafish) may also have osteogenic trunk neural crest cells [22,[24][25][26][27].…”

Three Ways to Tackle the Turtle: Integrating Fossils, Comparative Embryology, and Microanatomy

“…Metaplastic ossification had already been identified as the main mode of ossification in trionychid turtle shells, where the incorporation and transformation of preformed dermal soft tissue structures into the mineralized bone tissue is most obvious ). In contrast, in a recent review of integumentary structures by Vickaryous and Sire (2009), which was based on several other developmental studies (Gilbert et al 2001Cebra-Thomas et al 2007; summarized by Rieppel 2012), intramembraneous ossification (i.e., growth of bone spiculae into the surrounding soft tissue) was proposed to be the main mode of costal and neural development. Given these conflicting data and interpretations, here we propose that both metaplastic and intramembraneous ossification, to various degrees and at different stages in ontogeny, play a role in costal and neural formation.…”