The long-standing mystery of the evolution of the turtle shell has been resolved by researchers from the RIKEN Center for Developmental Biology in Kobe. The answer involves a folding process during embryonic development accompanied by a progression of relatively straightforward changes, not the major evolutionary leap that had previously been proposed.
Turtles, birds, mammals, lizards and crocodiles, known collectively as the amniotes, share a common ancestor. Compared with the other members of this group, however, the turtle skeleton seems inside out. The dorsal shell is generated by a fusing of the ribs, and the shoulder blade, or scapula, is contained inside the rib cage. In the other animals, the scapula is outside the rib cage.
Shigeru Kuratani and his colleagues thought the key to the evolution of this radical change may lie in the embryological development of the turtle. As detailed in a recent paper in Science1, they used tissue-specific stains and the activity of pivotal genes to compare the development of bones and muscles in Chinese soft-shelled turtles to equivalent embryonic stages in chickens and mice.
What they found was a delicate interplay of tissue folding and movement. In the chicken and mouse, the ribs grow out from the spinal column and follow the body wall around the sides to the chest of the developing animal forming a cage that leaves the shoulder blade outside. But the turtle ribs stop short, sticking straight out from backbone without bending. Then, a folding process occurs along the sides of the turtle pinching in the body wall between the ribs and the shoulder blade, leaving the ribs over and above the scapula. After the short turtle ribs and interspersed skin tissue fuse to form the bony dorsal shell, the fold forms its outer lateral extent.
Some of the muscular connections between the ribs and other parts of the skeleton remain intact during the folding process. But the resultant positioning of bones in the turtle has allowed other functional muscular connections to evolve. A 220-million-year-old turtle fossil discovered last year in China, which has a shell only on the underside, could easily represent an intermediate stage in development. “A developmental stage of the modern turtle, when the ribs have not encapsulated the shoulder blade yet, resembles this fossil species,” Kuratani says.
What causes the folding process in turtle development is unknown. “That will be the subject of a future study,” Kuratani says.
The corresponding author for this highlight is based at the Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology.
1. Nagashima, H., Sugahara, F., Takechi, M., Ericsson, R., Kawashima-Ohya, Y., Narita, Y. & Kuratani, S. Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325, 193–196 (2009).
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