Embryonic twist yields turtle shell

The bizarre body plan of turtles may be less of an evolutionary feat than scientists once believed. According to a linkurl:study;https://www.sciencemag.org/cgi/content/abstract/325/5937/193 published online today in Science, the unique organization of the ribs and the development of the unusual shell that turtles call home may be explained by a relatively small structural variation from their animal relatives that occurs during embryonic development. Image: Wikimedia commons"The turtle body plan

Written byJef Akst

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The bizarre body plan of turtles may be less of an evolutionary feat than scientists once believed. According to a linkurl:study;https://www.sciencemag.org/cgi/content/abstract/325/5937/193 published online today in Science, the unique organization of the ribs and the development of the unusual shell that turtles call home may be explained by a relatively small structural variation from their animal relatives that occurs during embryonic development.

Image: Wikimedia commons

"The turtle body plan was so enigmatic, so mysterious," said comparative embryologist linkurl:Shigeru Kuratani;https://www.cdb.riken.go.jp/en/02_research/0202_creative04.html of the RIKEN Center for Developmental Biology in Japan, who led the study, "but developmentally viewed, it's reasonable." These findings support the notion that morphological novelties can arise from relatively minor changes during embryonic development -- a view known as evolutionary development, or more colloquially, evo-devo, explained paleontologist linkurl:Olivier Rieppel;https://fm1.fieldmuseum.org/aa/staff_page.cgi?staff=rieppel of the Field Museum in Chicago, who was not involved in the research. "They show now how developmental steps [in the turtle] could have led to this initial formation" of the turtle's shell. In addition to the overt peculiarity of the turtle's shell, or carapace -- which is comprised of flattened ribs and vertebrae -- the shoulder blade, or scapula, is located beneath the shell, within the rib cage. That's the exact opposite of the configuration found in other amniotes. Scientists have long debated exactly how these skeletal features got transposed. By comparing developing embryos of turtles, chickens, and mice, Kuratani and his colleagues identified a straightforward developmental mechanism which likely spurred these seemingly drastic changes over the course of the turtle's evolutionary lineage. Kuratani examined embryos at a variety of developmental stages and, using histology, imunohistochemistry and in situ hybridization, identified developmental features in the musculoskeletal system that are unique to turtles. Early in development, turtles had subtle differences compared to the other organisms, such as shortened ribs, but the biggest differences came later, when all but the most anterior rib grew outward and forward, instead of curving around the body cavity. At the same time, the dorsal part of the body wall folded inward, causing the extending ribs to cover the scapula. Rieppel said the study takes "a very important step" in understanding the evolution of turtle morphology. "This is the first time that this body wall folding has been described," Rieppel said, "and [it] explains the initial stage of the [carapace formation] and the consequence it has for rib growth and development."

The scapula (red) is outside
ribs in the mouse and the chicken,
and inside the ribs in turtle.
Image: Shigeru Kuratani and
Hiroshi Nagashima

The team also traced the development of the muscles that join the scapula to the ribs and found that despite the structural transformations in the turtle's skeletal system, these muscles maintained their original connections during development, twisting to accommodate the skeletal changes. This suggests that the rib position in turtles is not entirely novel, but merely shifted, Kuratani explained. The turtle body plan still retains the structures and connections that are homologous to their ancestors. There were, however, changes to the connections made by turtle limb muscles. Muscle precursors that normally attach to the nearest part of the trunk instead grew around the main part of the carapace to attach to the plate closest to the turtle's head. "Limb muscles are exceptional," Kuratani said. "[They] tend to change connectivity rather radically." Comparing these embryonic stages of turtle development with a turtle fossil recently discovered in 220-million-year-old marine sediments in China, Kuratani could confidently say that "the [developing] modern turtle is recapitulating the ancestral turtle [lineage]." Indeed, while the ancient turtle lacked a complete carapace, it had the broadened, outward-extending ribs of modern turtles. Furthermore, the scapula remained outside the rib cage of this fossil, just like the early stages of modern turtle embryogenesis. Researchers' understanding of how the turtle evolved such a strange trait is "not compete just yet," said Rieppel, "but it's one more piece in the puzzle. [And] this is a very important piece in a very important puzzle."
**__Related stories:__***linkurl:Tentacles test tenets of evolution;https://www.the-scientist.com/blog/display/55198/
[18th November 2008]*linkurl:From lizard claw to mammal hair?;https://www.the-scientist.com/blog/display/55181/
[10th November 2008]*linkurl:To Effectively Discuss Evolution, First Define 'Theory';https://www.the-scientist.com/article/display/17546/
[12th May 1997]

Meet the Author

Jef Akst

Jef (an unusual nickname for Jennifer) got her master’s degree from Indiana University in April 2009 studying the mating behavior of seahorses. After four years of diving off the Gulf Coast of Tampa and performing behavioral experiments at the Tennessee Aquarium in Chattanooga, she left research to pursue a career in science writing. As The Scientist's managing editor, Jef edited features and oversaw the production of the TS Digest and quarterly print magazine. In 2022, her feature on uterus transplantation earned first place in the trade category of the Awards for Excellence in Health Care Journalism. She is a member of the National Association of Science Writers.

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