Skeletal development in the Chinese soft‐shelled turtle Pelodiscus sinensis (Testudines: Trionychidae)

Abstract

We investigated the development of the whole skeleton of the soft-shelled turtle Pelodiscus sinensis, with particular emphasis on the pattern and sequence of ossification. Ossification starts at late Tokita-Kuratani stage (TK) 18 with the maxilla, followed by the dentary and prefrontal. The quadrate is the first endoskeletal ossification and appears at TK stage 22. All adult skull elements have started ossification by TK stage 25. Plastral bones are the first postcranial bones to ossify, whereas the nuchal is the first carapacial bone to ossify, appearing as two unstained anlagen. Extensive examination of ossification sequences among autopodial elements reveals much intraspecific variation. Patterns of ossification of cranial dermal elements are more variable than those of endochondral elements, and dermal elements ossify before endochondral ones. Differences in ossification sequences with Apalone spinifera include: in Pelodiscus sinensis the jugal develops relatively early and before the frontal, whereas it appears later in A. spinifera; the frontal appears shortly before the parietal in A. spinifera whereas in P. sinensis the parietal appears several stages before the frontal. Chelydrids exhibit an early development of the postorbital bone and the palatal elements as compared to trionychids. Integration of the onset of ossification data into an analysis of the sequence of skeletal ossification in cryptodirans using the event-pairing and Parsimov methods reveals heterochronies, some of which reflect the hypothesized phylogeny considered taxa. A functional interpretation of heterochronies is speculative. In the chondrocranium there is no contact between the nasal capsules and planum supraseptale via the sphenethmoid commissurae. The pattern of chondrification of forelimb and hind limb elements is consistent with a primary axis and digital arch. There is no evidence of anterior condensations distal to the radius and tibia. A pattern of quasi- simultaneity is seen in the chondrogenesis of the forelimb and the hind limb.

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

“…Turtle skeleton formation has been studied in multiple species from hardshelled to soft-shelled turtles and from side-necked (Pleurodira) to hidden-neck turtles (Cryptodira) (33,(36)(37)(38)(39)(40). These studies have emphasized the development of the carapacial skeleton, following the order of mineralization of skeletal elements during late embryogenesis and comparing carapace development between different species of turtles.…”

Skeletal development in the African elephant and ossification timing in placental mammals

“…While previous studies have interpreted heterochrony only when events are reported using both optimization approaches, we have previously shown that Parsimov is overly conservative, and using either ACCTRAN or DELTRAN (not both) may be justified in some cases [19]. Furthermore, following Hautier et al [19] and Sánchez-Villagra et al [29], we performed additional Parsimov analyses with all ties converted to missing data (electronic supplementary material, S3 and S4) to control for the artefactual interpretation of heterochrony owing to accumulation of ties across events. We did not use the Pgi heterochrony search algorithm by Harrison & Larsson [30], as it is currently not programmed to analyse datasets with ties excluded [19].…”

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

“…As in other amniotes, the turtle shoulder girdle maintains its position relative to the muscle plate throughout development via a unique muscle folding mechanism, in some cases maintaining ancestral connectivities and in others creating novel ones [15]. However, the entire pectoral girdle remains anterior to the cartilaginous first dorsal rib throughout ontogeny, and only becomes encapsulated within the shell upon intramembranous ossification of the nuchal bone, the dorsal ribs and neural spines of the carapace [18]. Indeed, as has long been noted by skilled anatomists [19], the scapula remains anterior to the first dorsal rib even in adult turtles.…”