Turtle Shell EvoDevo


A few weeks ago there was a post here about the controversy over exactly what position turtles have in vertebrate evolution.  Turtles have long been considered anapsida reptiles (Romer 1966). Anapsids lack a temporal foramen and all of them, except the turtles (if in fact they are anapsids), were extinct by the Triassic. But, even Romer seemed to question whether or not turtles were really anapsids, he wrote:


“The turtles, forming the order Chelonia, may technically be included as members of the Anapsida, since the skull roof, although often emarginated and incomplete, has never developed true temporal openings. In almost every other respect, however, the turtles have departed widely from the structural pattern of their cotylosaur ancestor.”

Other hypotheses about turtle relationships were forth coming: Rieppel and deBraga (1996) suggested turtles belong to a sister-group to extant lepidosaurian diapsids (tuatars, lizards and snakes). But, molecular studies (most recently Hugall et al. 2007) have consistently suggested turtles have a close affinity to archosaurian diapsids (crocodilians and birds); a hypothesis also supported by some similarities of the karyotypes and genomes of sauropsidian lineages and turtles (Chapus and Edwards, 2009) and a view held by classical embryologists such as Ernst Haeckel and Gavin de Beer. Turtles have changed the pattern of their axial skeleton, placing their scapula inside the rib cage and fusing their ribs to the carapace (upper shell) making them a novelty. Attempts to understand this has created the variety of hypotheses.

 In a recent paper, Shigeru Kuratani of the RIKEN Center for Developmental Biology, in Kobe, Japan and colleagues propose the key to understanding the turtle’s shell patterning lies in the modification of the ribs. Turtle embryos have a unique structure, the carapacial ridge (CR). It is assumed to be responsible for the changes in the growth pattern that result in the turtle’s carapace. In turtle embryos growth of the ribs is arrested in the axial part of the body, this allows dorsal and lateral oriented growth to encapsulate the scapula. Although the CR does not appear to induce this axial arrest, it has been shown to support the fan-shaped patterning of the ribs, which occurs at the same time as the marginal growth of the carapace along the line of the turtle-specific folding that takes place in the lateral body wall. During the process of folding, some trunk muscles maintain their ancestral connections, while the limb muscles establish new attachments specific to the turtle. Kuratani et al. suggest the turtle body plan can thus be explained with our knowledge of vertebrate anatomy and developmental biology, and that it is consistent with the evolutionary origin of the turtle suggested by the recently discovered fossil species, Odontochelys – the very unique turtle with only the lower shell (plastron) - lower art work.


Literature
Chapus, C., and Edwards, S. V. 2009. Genome evolution in Reptilia: in silico chicken mapping of 12,000 BAC-end sequences from two reptiles and a basal bird. BMC Genomics 10 (suppl 2): S8.

Kuratani, S., S. Kuraku, H. Nagashima. 2011. Evolutionary developmental perspective for the origin of turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge. Evolution & Development 13(1):1-14.


Rieppel, O., and deBraga, M. 1996. Turtles as diapsid reptiles. Nature 384:453–455.

Romer, A. S. 1966. Vertebrate Paleontology. 3rd Ed. University of Chicago Press, Chicago.

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