A developmental staging system and musculoskeletal development sequence of the common musk turtle (Sternotherus odoratus)

Abstract

Background: The extremely derived body plan of turtles has sparked a great interest in studying their developmental biology. Here, we describe the embryonic development of the Stinkpot, or common musk turtle (Sternotherus odoratus), a small aquatic turtle from the family Kinosternidae. Results: We identify 20 distinct developmental stages, some comparable to stages described by previous studies on other turtles and some in between these, improving the resolution of the generalities of turtle development. We provide a detailed account of both the external morphology and skeletal development, as well as a general look at the early stages of muscular development until the attainment of the adult muscular anatomical pattern. Conclusions: Several potential skeletal and muscular apomorphies of turtles are identified or elaborated. The musk turtle, with its small size and hardshelled egg, could become an important species for the study of turtle evolution and development, suitable for in ovo experimentation and late stage imaging of well-advanced anatomical features.

Skeletal development of Kinosternon scorpioides limbs (Chelonia: Kinosternidae)

“…This pattern was reported for most studies, including this one (Burke & Alberch, 1985;Sheil, 2003;Sheil & Greenbaum, 2005;Werneburg et al, 2009;Smith-Paredes et al, 2020). Moreover, at the end of embryonic Stage 18 in K. scorpioides, the chondrification of all limb elements is observed (Sánchez-Villagra et al, 2009;Sheil, 2003;Sheil, 2005;Sheil & Portik, 2008;Smith-Paredes et al, 2020). Our findings show that there is already a structure at this stage that will give rise to future ossifications.…”

“…Therefore, the ossification process in K. scorpioides begins in the long bones of the stylopodium and zeugopodium. This is followed by the metacarpals and tarsals, phalanges, and carpal and tarsal regions in the proximal-distal direction, as observed for the species of the families Trionychidae, Chelydridae, Cheloniidae, Chelidae, and Kinosternidae (Bona & Alcalde, 2009;Lima et al, 2016;Sánchez-Villagra et al, 2007;Sheil, 2003;Sheil, 2005;Smith-Paredes et al, 2020;Werneburg et al, 2009). In contrast, our results differ from those observed in P. expansa (Sheil & Greenbaum, 2005;Vieira et al, 2011), where phalanges ossification is distal-proximal.…”

“…However, detailed information on their ossification and anatomy was not provided. In addition, the external and musculoskeletal development of S. odoratus was assigned 20 stages of morphological progression (Smith‐Paredes, Lord, Meyer, & Bhullar, 2020).…”

“…The Kinosternidae family appeared at approximately 50 Ma (Joyce, Parham, et al, 2013) and has conservative anatomical characteristics compared to other embryological research animal models, such as sea turtles and red‐eared slider turtles. Recently, Smith‐Paredes et al (2020) defended their use of Kinosternid S. odoratus as an experimental model, because like the other representatives of the family it has characteristics that facilitate laboratory handling, such as being small in size and having eggs with a hard shell. The Brazilian representative species of Kinosternidae family, Kinosternon scorpioides , is a chelonian whose natural stocks are overexploited.…”

Musculoskeletal Development, Maintenance and Regeneration: Part One

“…Scaal also discusses evolutionary adaptations in rib development in snakes and turtles, which resulted in the expansion of the ribs along the body axis in snakes and the formation of the hard turtle shell, the carapace. Smith‐Paredes et al 4 continue on the theme of turtles by describing the staging and development of the common musk turtle, Sternotherus odoratus (also known as Stinkpot), a new model for understanding developmental processes. The advantages of “Stinkpot” embryos as a model system are that they develop within a hard shell, enabling windowing and easier experimental manipulation, and that their small size allows whole‐mount visualization of tissues by confocal microscopy, which the authors demonstrate by imaging the differentiated musculature.…”