by Greg Mayer
In a paper soon to be published in Current Biology (abstract), Tyler Lyson and colleagues propose a model for the origin of turtles, using the Permian (ca. 260 mya) fossil Eunotosuarus as a transitional form.
The origin of turtles is a fascinating and important area of study, although one that is perhaps generally underappreciated (Burke 2009). The reason for its importance is that the turtle shell is probably the most novel and highly derived of all skeletal structures in the vertebrates. Nothing in human evolution, for example, compares. What do we have that’s distinctive? A really short tail? It’s been done to death, and just involves some reduction in size and number of bones. Bipedality? Also done many times. A large cranium? Just a few bones getting bigger.
What have turtles done? They’ve moved their shoulder and pelvic girdles inside their rib cages! If you want to appreciate what this means, reach behind your back and touch your shoulder blades, then reach down and touch your hip bones. Now feel your ribcage, front and back. And now imagine getting your shoulder blades and hips inside your rib cage– that’s what turtles have done.
Understanding of the origin of turtles has been hampered by the lack of a good fossil record. For many years the earliest known turtle was Proganochelys from the Late Triassic (ca. 210 mya), which, while primitive in various respects, had a full shell, both top (carapace) and bottom (plastron). The first fossil breakthrough came in 2008, when Li and colleagues described Odontochelys, a Late Triassic turtle a bit older than Proganochelys, but in which the plastron was well formed, but the carapace (top) consisted of only neural bones above the vertebrae, and enlarged ribs.
Lyson and colleagues extend the model of shell origins, incorporating further data on shell ontogeny in modern turtles, and, most significantly adding Eunotosaurus as an early ancestral turtle, which has a proto-carapace of expanded ribs. They also point to Milleretta, another Permian reptile, as a possible very first step in the direction of turtles. (At this point, we pause for Snappy to say hello, so readers don’t forget what the object of our discussion is.)
There are two phylogenetic controversies that are involved in this scenario of turtle origin. First, although Eunotosaurus has long been bandied about as a turtle precursor, the consensus has long been that it is not, although Lyson and colleagues (2010) have argued it is. Second, there is great debate about where turtles fit in amongst reptiles in general. Because of the generally primitive nature of their skulls (lacking any openings or fenestrations), turtles have often been linked with one or another of various early reptile groups, and Lyson and colleagues favor this view. There is an almost equally old hypothesis, however, that turtles, despite lacking any skull openings, are nonetheless members of the Diapsida, the great group of two-fenestra reptiles (and their modern feathery descendants) that includes Archosaurs (crocodiles and birds among living taxa, dinosaurs and pterosaurs among the extinct) and Lepidosaurs (tuatara, lizards and snakes among living taxa, mosasaurs among the extinct).
Recent molecular data, including two new genome studies (Wang et al. 2013, Shaffer et al. 2013; see Gilbert and Corfe 2013), have supported earlier molecular studies (including one of my own) in placing turtles among the Diapsida, and indeed, well within the Diapsida, as the sister group of the extant archosaurs. Although the resolution of these latter debates will have bearing on the full turtle origin story, one thing that I think is now clear is the stepwise origin of the turtle shell, with the various components having been assembled sequentially.
Burke, A.C. 2009. Turtles… …again. Evolution & Development 11:622-624.
Gilbert, S.F. and I. Corfe. 2013. Turtle origins: picking up speed. Developmental Cell 25:326-328.
Kirsch, J.A.W. and G.C. Mayer. 1998. The platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory. Philosophical Transactions of the Royal Society B 353:1221-1237. pdf
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. abstract
Lyson, T.R., G.S. Bever, B.S. Bhullar, W.G. Joyce, and J.A. Gauthier. 2010. Transitional fossils and the origin of turtles. Biology Letters 6:830-833. pdf
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 in press. abstract
Shaffer, H.B. et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biology in press. pdf
Wang, Z., et al. 2013. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nature Genetics 45 701-706. pdf