The Origin of Turtles: Why Was Stephanospondylus Forgotten?

UPDATED SEPT 29, 2013 and APRIL 08, 2014

A turtle is side view.

Figure 1. A turtle in lateral view. Image from the Encarta website.

Paleontologists can’t seem to figure out where turtles fit on the reptile family tree. Not with morphology. And not with DNA. Some posit a terrestrial origin. Others say aquatic.

Morphology
Hedges and Poling (1999) reported, “The classical phylogeny of living reptiles pairs crocodilians with birds, tuataras with squamates, and places turtles at the base of the tree.” Traditionally, turtles were regarded as living ‘stem’ amniotes despite having an extremely derived morphology: fused skull bones, toothless and a shell to call their home. Turtles were proposed to be sisters to all other living amniotes (Gaffney 1980) largely because they had no temporal fenestra.

Then computer-assisted phylogenies began to be published.

Owenetta

Figure 2. Owenetta in various views.

Procolophonid Origins?
Reisz and Laurin (1991) and Laurin and Reisz (1995) proposed a procolophonid origin for turtles when they described new specimens of Owenetta. In the present large study (see below) Owenetta is not close to Procolophon, but nests closer to the origin of Lepidosauriformes.

Anthodon

Figure 3. Anthodon in various views from Lee (1997).

Pareiasaur Origins?
Lee (1997) nested the pareiasaur, Anthodon, closer to turtles than any other included taxon. The scapula of Anthodon included an acromion process and small dermal ossicles covered the body. Unfortunately, like all pareiasaurs, Anthodon had flaring cheeks (quadratojugals), a reduced tail and other characters that would have removed it from the actual ancestry of turtles. Still Anthodon is very close to turtles in the present large study (see below).

Placochelys

Figure 4. Placochelys, a placodont and a sauropterygian.

Sauropterygian Origins?
deBraga and Rieppel (1997) proposed a relationship to sauropterygians in general (failing to produce a specific sister genus). All lepidosaurs (lizards and sphenodontians) nested as an outgroup. Within Sauropterygia, certain placodonts did have a carapace and plastron (see above), but these were clearly developed by convergence with turtles. These taxa undoubtedly affected results as also documented here. In the present analysis (see below) sauropterygians are not related to turtles or lepidosaurs.

DNA
Hedges and Poling (1999) nested turtles with crocodilians by comparing their DNA. More recently, using refined methods, Lyson et al. (2011) nested turtles with lizards, duplicating the present analysis (see below). Virtually all paleontologists consider both crocodilians and lizards to be “diapsids” with a common ancestor in Youngina. That relationships is not supported here (see below) as crocodilians nest very far from lizards. However the Lyson et al. nesting of turtles close to lizards is supported.

Proganochelys. Formerly the most primitive turtle.

Figure 5. Proganochelys. Formerly the most primitive turtle.

Proganochelys
For over a hundred years, until the discovery of Odontochelys (see below), Proganochelys (Baur 1887) had been known as the oldest and most primitive turtle. It lived during the Late Triassic, 205 mya. It had the classic turtle shape with a complete carapace and plastron and was largely toothless, but retained palatal teeth. A row of spikes topped the neck and tail, neither of which could withdraw beneath the protection of the shell.

Figure 1. Click to enlarge. Odontochelys the quasi-turtle in dorsal, lateral and ventral views. The same for the skull.

Figure 1. Click to enlarge. Odontochelys the quasi-turtle in dorsal, lateral and ventral views. The same for the skull.

Odontochelys
The discovery of an older, more primitive turtle, Odontochelys (Li et al. 2008), the first turtle with teeth, prompted reexamination of the data. It lived during the Late Triassic, 225 mya. The carapace was reduced in the manner of soft-shelled turtles, but Odontochelys was not directly related to them. Found in marine sediments, Odontochelys reignited hypotheses of an aquatic, sauropterygian origin for turtles (see above).

Figure added. Elginia is a stem turtle. Meiolania is a basal turtle. Both have horns.

Figure added. Elginia is a stem turtle. Meiolania is a basal turtle. Both have horns.

Elginia and Meiolania
The stem turtle Elginia and the basal turtle Meiolania demonstrate the loss of teeth and provide some clue to the post-crania of the skull-only taxon of Elginia.

Reptile family tree

A Larger Dataset
The large present tree of 586 taxa provided a fully resolved nesting of turtles with Stephanospondylus, pareiasaurs, Sclerosaurus, Elginia and turtles (Meiolania) in order of increasing distance. Both overall and in fine detail, no other taxa on this list come closer to turtles.

Figure 8. Click to enlarge. Stephanospondylus based on parts found in Stappenbeck 1905. Several elements are re-identified here. Note the large costal plates on the ribs, as in Odontochelys. The pubis apparently connected to a ventral plastron, not preserved. The interclavicle was likely incorporated into the plastron.

Figure 8. Click to enlarge. Stephanospondylus based on parts found in Stappenbeck 1905. Several elements are re-identified here. Note the large costal plates on the ribs, as in Odontochelys. The pubis apparently connected to a ventral plastron, not preserved. The interclavicle was likely incorporated into the plastron.

Stephanospondylus – Practically Forgotten
No modern analyses have included Stephanospondylus (Geinitz and Deichmuller 1882), which was widely considered a diadectid and a possible juvenile. Romer (1925) provided figures for this study. Stephanospondylus lived some 290 million years ago, at least 65 million years prior to Odontochelys. That gave time for the ancestors of Odontochelys to produce and reduce the carpace. No shell is associated with Stephanospondylus, but it had some teeth similar to those of Odontochelys while the posterior teeth were expanded like molars, as in other diadectids. Originally considered a diadectid, Stephanospondylus had certain basal pareiasaur traits, including an acromion process on the scapula. Stephanospondylus branched off the base of the pareiasauria prior to the development of flaring cheeks and likely remained rather small. It was also derived from Milleretta, separate and convergent with Odontochelys.

Certainly closer relatives to turtles will be found someday to bridge the 65 million year gap between Stephanospondylus, but at present, Stephanospondylus is the closest known taxon to turtles, closer than Odontochelys. By the way, as a test, you can lose Stephanospondylus and several other closest sister taxa and turtles will still not shift from their nesting site. I was even able to remove all taxa, except the basal pterosaur, and turtles refused to budge.

Why Was Stephanospondylus Forgotten?
Stephanospondylus has not been included in recent studies and analyses on turtle origins because it has been considered a diadectid related to Diadectes. The best specimen is also a scrappy fossil based on bits and pieces. Currently diadectids are considered pre-amniotes, non-reptiles, and turtles are definitely amniotes and reptiles. However, the current heretical family tree of the reptiles and their non-reptile ancestors (Figure 7) nests diadectids firmly and deeply within the Reptilia. So, parenthetically, but not directly, diadectids are part of the story why Stephanospondylus has not been considered as a turtle ancestor previously. 

 

References:
Baur G 1887. On the phylogenetic arrangement of the Sauropsida: Journal of Morphology, v. 1, n. 1:93-104.
deBraga M and Rieppel O 1997. Reptile phylogeny and the interrelationships of turtles. Zool. J. Linn. Soc. 120, 281–354.
Gaffney ES 1980. Phylogenetic relationships of the major groups of amniotes. In The terrestrial environment and the ori- gin of land vertebrates (ed. A. J. Panchen), pp. 593–610. Lon- don: Academic Press.
Gaffney ES 1990. The comparative osteology of the Triassic turtle Proganochelys, Bull. Am. Mus. Nat. Hist. 194: 1–263.
Geinitz HB and Deichmüller JV 1882. Die Saurier der unteren Dyas von Sachsen. Paleontographica, N. F. 9:1-46.
Hedges SB and Poling LL 1999. A Molecular Phylogeny of Reptiles. Science 283 no. 5404 pp. 998-1001. DOI: 10.1126/science.283.5404.998
Kissel R 2010. Morphology, Phylogeny, and Evolution of Diadectidae (Cotylosauria: Diadectomorpha). Toronto: University of Toronto Press. pp. 185. online pdf
Laurin M and Reisz, RR 1995.
A reevaluation of early amniote phylogeny. Zoological Journal of the Linnean Society 113, 165–223.
Lee MSY 1997. Pareiasaur phylogeny and the origin of turtles. Zoological Journal of the Linnean Society 120: 197-280.
Li C, Wu X-C, Rieppel O, Wang L-T and Zhao L-J 2008. An ancestral turtle from the Late Triassic of southwestern China Nature, 456 (7221), 497-501 DOI: 10.1038/nature07533
Lyson TR, Sperling EA, Heimberg AM, GauthierJA, King BL, and Peterson KJ 2011. MicroRNAs support a turtle + lizard clade. Biol Lett 2011 : rsbl.2011.0477v1-rsbl20110477.abstract – online news story
Reisz RR and Head JJ 2008.Palaeontology: Turtle origins out to sea Nature, 456 (7221), 450-451 DOI: 10.1038/456450a
Reisz R R and Laurin M 1991. Owenetta and the origin of turtles. Nature 349, 324–326.
Romer AS 1925. Permian amphibian and reptilian remains described as Stephanospondylus. Journal of Geololgy 33: 447-463.
Stappenbeck R 1905. Uber Stephanospondylus n. g. und Phanerosaurus H. v. Meyer: Zeitschrift der Deutschen Geologischen Gesellschaft, v. 57, p. 380-437.
wiki/Odontochelys
wiki/Proganochelys
wiki/Stephanospondylus

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