On the carapacial ridge in turtle embryos: its developmental origin,function and the chelonian body plan

Abstract

The chelonian carapace is composed of dorsolaterally expanded ribs; an evolutionary change in the rib-patterning program is assumed to be related to this novelty. Turtle embryos exhibit a longitudinal ridge called the carapacial ridge (CR) on the flank, and its histological resemblance to the apical ectodermal ridge of the limb bud implies its inductive activity in the unique patterning of the ribs. We studied the Chinese soft-shelled turtle, Pelodiscus sinensis, and confirmed by labeling with a lipophilic dye, DiI, that the CR contains the somite-derived dermis and that it is a unique structure among amniotes. Using electroporation of a dominantnegative form of LEF-1, the CR-specific gene, we showed that CR-specific genes function in the growth and maintenance of the CR. Microcauterization or implantation of the CR did not change the dorsoventral pattern of the ribs, and only their fan-shaped pattern was arrested by CR removal. We conclude that the CR is a true embryonic novelty among amniotes and, because of the specific expression of regulatory genes, it functions in the marginal growth of the carapacial primordium, thereby inducing the fan-shaped arrangement of the ribs.

The origin and loss of periodic patterning in the turtle shell

“…3B; supplementary materials and methods). This initial condition follows from the observation of a pre-pattern of 12 marginal scute placodes on each carapacial ridge that we hypothesize to be established by the somites, the segmental units of paraxial mesoderm on either side of the neural tube and notochord in vertebrate embryos (Yntema, 1970;Nagashima et al, 2007;Moustakas, 2008). We identified this pre-pattern with the sequentially alternating expression domains of Gremlin-Shh-Bmp in the carapacial ridge that are shown in Fig.…”

“…Recent studies of turtle development and paleontology (CebraThomas et al, 2005;Nagashima et al, 2007;Li et al, 2008;Moustakas, 2008;Sánchez-Villagra et al, 2009;Kawashima-Ohya et al, 2011;Kuratani et al, 2011;Hirasawa et al, 2013) have advanced our understanding of the evolutionary origin of turtles and the genetic and cellular interactions that regulate various aspects of bone development in the carapace. However, the genetic regulation of the origin and evolution of the epidermal scutes has not been addressed.…”

Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge

“…The CR is a bulge of thickened ectoderm overlaying a condensed mesenchyme that first appears in the lateral trunk, dorsal to the lateral somitic frontier running anterior-posteriorly along the flank region, and it has been proposed to be important for directing the shell development (Burke, 1989, Cebra-Thomas et al, 2005, Nagashima et al, 2007. The CR first appears during stage TK14 (according to the staging table of the Chinese soft-shell turtle, Pelodiscus sinensis - Tokita and Kuratani, 2001-; equivalent to stages Yntema 14 of Chelydra serpentina -Yntema, 1968-;and Greenbaum 15 of the hard-shell red-eared slider Trachemys scripta -Greenbaum, 2002-).…”

“…Among these genes, Lef-1 is encoding a transcriptions factor that functions as an effector of the canonical Wnt signaling pathway (Behrens et al, 1996). Interestingly, Lef-1 seems to have an important role in controlling the horizontal (not dorsoventral) orientation of the ribs in the carapace (Nagashima et al, 2007). Furthermore, APCDD1 is known to be a target of the canonical Wnt pathway.…”

Pushing the frontiers of development

“…He presented a novel and exciting approach that uses sub-micron resolution synchrotron scans to map muscle attachments to fossil bones in 3D that holds great promise for soft-tissue reconstructions in many other contexts. Shigeru Kuratani (RIKEN Center for Developmental Biology, Kobe, Japan) discussed the ribderived turtle carapace as an evolutionary novelty, which results from the arrest and dorsolateral confinement of rib growth, leading to a turtle-specific infolding of the lateral body wall (Nagashima et al, 2007). He showed that the carapacial ridge -a turtle-specific structure that lies along the line of infolding -does not play an inductive role in carapace patterning as previously thought, but instead appears to have co-opted elements of the Wnt signaling pathway for the control of carapace growth.…”