Who are the turtles? Vertebrate paleontology helps to solve a long-standing puzzle.

Turtles are reptiles that are instantly recognizable. Their iconic shell has made them well-protected from predators and from paleontologists trying to understand their place on the reptile family tree. For as long as they have been studied, turtles have been recognized as reptiles, but exactly what sort of reptiles they were has been difficult to uncover. To understand why, we have to broaden our scope a bit and examine the amniotes.

Amniotes are those vertebrates whose embryos produce four life-supporting membranes that allow development inside a shelled egg or within the wall of the mother’s uterus. Thus, amniotes include the reptiles (of which birds are members) and mammals. The earliest amniotes (~310 Ma) had a skull with just two sets of openings: the nostrils and the orbits, and the braincase region of the skull was solid bone (Benton, 2005; Pough et al., 2013). However, soon after their appearance, the amniotes diverged into the reptile- and mammal-lines, and along with these splits came the appearance of openings posterior to the eye called temporal fenestrae. In the reptile-line amniotes, many members developed two temporal fenestrae on either side of the skull, whereas in mammal-line amniotes a single temporal fenestra developed on either side (Benton, 2005; Pough et al., 2013). The appearance of these openings has a complex origin that probably resulted from competing selective forces tied to jaw muscle expansion and skull lightening (Liem et al., 2001; Benton, 2005; Pough et al., 2013). Regardless, most reptiles have what is called the diapsid condition and possess two temporal fenestrae.

What about turtles? All extant turtles have no discernable temporal fenestrae, giving them what is traditionally called an anapsid skull. Based primarily on this feature, and the fact that turtle anatomy is so weird that the origins of various features are difficult to trace through the fossil record, it was hypothesized that turtles were the last remaining vestige of a primitive branch of reptiles called the parareptiles. Moreover, until recently, the earliest recognized turtle fossil was Proganochelys from the Triassic of Germany (~210 Ma), which already had all of the major hallmarks of turtles, including an anapsid skull and a shelled body (Gaffney and Meeker, 1983; Gaffney, 1990). Thus, for a good part of the 20th century, turtles were considered a primitive branch of the Reptilia far removed from the other diapsid reptiles.

Cracks in the foundation of the parareptile/anapsid origins of turtles hypothesis began to accumulate in the 1990s and into the 21st century. Restudy of turtle embryonic development revealed that they shared many similarities with other diapsid reptiles (DeBraga and Rieppel, 1997; Rieppel and Reisz, 1999). One evolutionary mystery had always been that turtles had their shoulder blades inside their ribcages, not on the outside like all other tetrapods. It had been proposed that the armor scutes of some parareptiles (which become progressively more armored) could have migrated forwards along with the ribs over time, swallowing up the shoulder blade in the process (e.g., Lee, 1997). However, developmental studies of the turtle shell clearly showed that the shoulder blade of turtles ends up inside the ribcage because the ribs grow outwards rather than downwards (Sánchez-Villagra et al., 2009; Kuratani et al., 2011; Hirasawa et al., 2013), breaking yet another link of turtles to the parareptiles. Finally, the past 20 years have seen the discovery of several new turtle fossils older than Proganochelys, many of which show traits tantalizingly similar to those of other diapsid groups (e.g., Li et al., 2008; Schoch and Sues, 2015).

Could it be that turtle skulls were once diapsid but secondarily lost their temporal fenestrae? The answer now appears to be yes. Two new discoveries point the way. The first is a new discovery by Bever and colleagues of new anatomical information from an old fossil reptile. Eunotosaurus is known from several specimens from the Permian (~260 Ma) of South Africa. Its body is fat and wide, and its ribs are expanded, an anatomy that presages the modern turtle condition where expanded ribs fuse with other tissues into a shell (Lyson et al., 2013). Intriguingly, the skull anatomy of Eunotosaurus has remained understudied. Using new CT-scanning techniques, Bever et al. (2015) have not only shown that Eunotosaurus had a large lower temporal fenestra, but a juvenile specimen clearly showed a distinctive upper temporal fenestra as well! In any other reptile, this would be regarded as evidence of a diapsid skull and placement among the diapsid reptiles. What of the adult skull? When adult specimens were scanned, the upper temporal fenestra was overgrown by bone, but when that bone was digitally “removed,” an unmistakable upper temporal fenestra was still there, hiding underneath. In a stroke, the skull of Eunotosaurus unequivocally shows that turtles descended with modification from diapsid reptiles.

Bridging the gap between Eunotosaurus and other fossil turtles is another new discovery by Schoch and Sues (2015) of a morphologically intermediate turtle named Pappochelys from the Middle Triassic (~240 Ma). Pappochelys has expanded ribs and robust gastralia (“belly ribs”) that appear to be the precursor to the plastron, the belly-piece of the shell in turtles. Moreover, Pappochelys, too, has small upper and lower temporal fenestrae, further evidence that turtles can indeed trace their ancestry back, not to the parareptiles, but among the diapsids instead.

Many turtle mysteries still remain. Chief among them is where among the diapsid reptiles do turtles belong? Here, the data from morphology and molecules continues to provide conflicting answers. Morphological data strongly supports affinities with lizards and kin, and possibly some of the marine reptile groups (sauropterygians), whereas molecular data fairly consistently place turtles as a sister group to the archosaurs. Another wrinkle in the turtle story is whether the shell itself first evolved on land or in the water. One thing is certain: the odd anatomy of turtles has served them well, and has made them both a success story and a general headache for those attempting to unravel their relationships.

Posted by: Matthew F. Bonnan, Stockton University

References Cited

Benton, M. J. 2005. Vertebrate Palaeontology, 3rd ed. Blackwell Publishing, Oxford, UK, 455 pp.

Bever, G. S., T. R. Lyson, D. J. Field, and B.-A. S. Bhullar. 2015. Evolutionary origin of the turtle skull. Nature.

DeBraga, M., and O. Rieppel. 1997. Reptile phylogeny and the interrelationships of turtles. Zoological Journal of the Linnean Society 120:281–354.

Gaffney, E. S. 1990. The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the AMNH; no. 194. .

Gaffney, E. S., and L. J. Meeker. 1983. Skull morphology of the oldest turtles: a preliminary description of Proganochelys quenstedti. Journal of Vertebrate Paleontology 3:25–28.

Hirasawa, T., H. Nagashima, and S. Kuratani. 2013. The endoskeletal origin of the turtle carapace. Nature Communications 4:2107.

Kuratani, S., S. Kuraku, and 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 13:1–14.

Lee, M. S. Y. 1997. Pareiasaur phylogeny and the origin of turtles. Zoological Journal of the Linnean Society 120:197–280.

Li, C., X.-C. Wu, O. Rieppel, L.-T. Wang, and L.-J. Zhao. 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497–501.

Liem, K., W. Bemis, W. Walker, and L. Grande. 2001. Functional Anatomy of the Vertebrates an Evolutionary Perspective. Thomson Brooks/Cole, Belmont (Calif.), 703 pp.

Lyson, T. R., G. S. Bever, T. M. Scheyer, A. Y. Hsiang, and J. A. Gauthier. 2013. Evolutionary Origin of the Turtle Shell. Current Biology 23:1113–1119.

Pough, F. H., C. M. Janis, and J. B. Heiser. 2013. Vertebrate Life, 9th ed. Pearson, Boston, 720 pp.

Rieppel, O., and R. R. Reisz. 1999. The origin and early evolution of turtles. Annual Review of Ecology and Systematics 1–22.

Sánchez-Villagra, M. R., H. Müller, C. A. Sheil, T. M. Scheyer, H. Nagashima, and S. Kuratani. 2009. Skeletal development in the Chinese soft-shelled turtle Pelodiscus sinensis (Testudines: Trionychidae). Journal of Morphology 270:1381–1399.

Schoch, R. R., and H.-D. Sues. 2015. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature. doi:10.1038/nature14472

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