In comparison to Proganochelys (Gaffney, 1990), Odontochelys semitestacea is a small turtle. The adult status of the specimen is documented not only by the generally well-ossified appendicular skeleton with a fully differentiated morphology of humerus and femur, but particularly by the fusion of the astragalus and calcaneum in the paratype (the elements meet in a closed suture in the holotype). In contrast, the astragalus and calcaneum uniformly form rounded, separate ossifications in marine reptiles subject to skeletal paedomorphosis (e.g., Rieppel, 2000, and references therein). The occurrence of skeletal paedomorphosis in marine reptiles also raises the question whether the carapace of Odontochelys is reduced rather than primitively incomplete. Reduction of the carapace in fossil and extant turtles, both in fresh water and marine species, shows variable patterns but never the one observed in Odontochelys, with broadened ribs that resemble the embryonic morphology of the ribs in extant turtles at a stage before nuchal, pygal, and marginal plates start ossification (e.g., Zangerl, 1939; Pritchard, 2008, and references therein). Carapace reduction is also generally correlated with reductions in the plastron, resulting in fontanelles much wider than the narrow gap that separates the left and right meso- and hypoplastra in Odontochelys. Finally, in all turtles, including Proganochelys (Gaffney, 1990), with a fully formed or reduced carapace, the neural arches of the dorsal www.nature.com/nature 1
vertebrae have shifted forwards by half a segment (Goette, 1989). This results in an articulation of the dorsal ribs at a level in between successive dorsal centra (Rieppel and Reisz, 1999). The result is an intercalation of neural and costal plates which presumably strengthens the carapace. Odontochelys is the only turtle known, fossil or extant, in which the dorsal ribs articulate in a facet located on the middle of the centrum as in other reptiles, which further documents its primitive status. To test the phylogenetic relationships of Odontochelys within turtles, we coded the new taxon for the data matrix published by Joyce (2007). We reversed the polarity of character 118 (tail club: absent = 0; present = 1), and coded character 120 for the presence of a dorsal epiplastral process irrespective of its putative homology with a clavicle (Gaffney, 1990), or cleithrum (Joyce et al, 2006; see discussion in Rieppel, 2008). The character coding for Odontochelys is as follows (in groups of five): 000??????? 0???0?????????????????0?0??00????0? 00???????????????????????????? 00???????0 00????????????? 00000???????0???0000??000 0??0? 0?00?? The data matrix was analyzed using PAUP* 4.0b10 for Macintosh. The analysis was rooted on the hypothetical all-0-ancestor (Joyce, 2007), and the rogue taxa identified by Joyce (2007), i.e., Portlandemys, Sandowina, and Mongolemys, were excluded. A heuristic search yielded 6244 equally parsimonious trees with a tree-length of 354 steps. The strict consensus tree shows Ondontochelys www.nature.com/nature 2
Proganochelys, Proterochersis, Palaeochersis, Australochelys, and a clade containing all other turtles included in the analysis in a basal polytomy. However, in 62% of the trees, Proganochelys is sister-taxon of a clade that comprises Odontochelys and all other turtles included in the analysis. If only one character is added (carapace absent in the hypothetical ancestor and in Odontochelys, present in all other turtles), the heuristic search yields 2401 equally parsimonious trees with a TL = 355, of which 100% show Odontochelys to be the sister-taxon of a clade comprising Proganochelys and all other turtles. The absence of a carapace is only one of several features by which Odontochelys is plesiomorphic relative to all other turtles, including Proganochelys. Coding these characters (i.e., presence of teeth on upper and lower jaws; relatively long preorbital skull; distinct transverse process of the pterygoid; dorsal rib articulation; long tail; absence of an acromial process; free sacral ribs; free caudal transverse processes; presence of a radiale (polymorphic); four phalanges in digits III and IV of manus and pes; and absence of osteoderms) would further reinforce that same signal. Odontochelys is thus shown to be the basal-most of all known turtles, fossil or extant. To test the position of turtles amongst reptiles in general, we included Odontochelys in the data matrix of Rieppel and Reisz (1999). In light of the fact that Odontochelys shows carapace formation to result from intramembranous ossification in the carapacial disc, rather than from fusion of body-osteoderms, we re-coded Testudines in that matrix for the absence of body-osteoderms (character 165: 2 0). We also added a character (#169) for plastron absent (0), present (1). Both Testudines www.nature.com/nature 3
and Odontochelys were coded for the absence of an upper temporal fenestra (character 50). We coded Odontochelys for the absence of a cleithrum (character 113), in light of the fact that there is no trace of a suture between the entoplastron and its dorsal process, and also taking into account that the evidence for the presence of a cleithrum in Kayentachelys (Joyce et al., 2006) is equivocal (as discussed in Rieppel, 2008). However, coding Testudines and Odontochelys for the presence of a cleithrum had no effect on the tree topology, but increased tree length by one step (reversal for the presence of a cleithrum in Odontochelys and turtles). The coding for Odontochelys is as follows (in groups of five):????????0????1????2??????????????????1?0??????0??0?????????????????????00?1?0??????????????1??1 01010 0?1?0?1001 111???20???0?01??121 111?0???1??0111 11111 00?11 0?2?1 10010?0?1 Rooting the analysis on an hypothetical all-0-ancestor, the heuristic search in PAUP* 4.0b10 for Macintosh yielded two equally parsimonious trees with a tree length of 609 steps, an ensemble consistency index of 0.3482, and a retention index of 0.7046. Using Seymouridae and Diadectomorpha as outgroups instead, the heuristic search yielded a single most parsimonious tree with a tree length of 608 steps, an ensemble consistency index of 0.3520, and a retention index of 0.6960. The tree topology is the same as that in Rieppel and Reisz (1999, fig. 1), except for the addition of Odontochelys. The latter comes out as sister taxon of Testudines, the two forming a clade that is the sister-group of Sauropterygia within Lepidosauromorpha. www.nature.com/nature 4
We do not, in this paper, consider Priscochelys hegnabrunnensis from the Muschelkalk (lower Ladinian, Middle Triassic) of Germany. This is a very incomplete dermal armor fragment of controversial interpretation, either as the world s oldest turtle (Joyce and Karl, 2006), or as a placodont (Scheyer, 2008). Disregarding Priscochelys for this reason, Odontochelys is the oldest known unquestionable turtle of lower Carnian age. The dating of the Wayao Member of the Falang Formation that yielded Odontochelys is based on biostratigraphical analysis, with ammonites and conodonts serving as index fossils (Sun et al. 2003; Xu et al., 2003) References Gaffney, E.S. The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the American Museum of Natural History 194, 1-263 (1990). Goette, A.. Über die Entwicklung des knöchernen Rückenschildes (Carapax) der Schildkröten. Zeitschrift für wissenschaftliche Zoologie 66, 407-434 (1899). Joyce, W. G., Jenkins, F. A. & Rowe, T. The presence of cleithra in the basal turtle Kayentachelys aprix. Fossil Turtle Research 1, 93-103 (2006). Joyce, W. G. & Karl, H.-V. The world s oldest fossil turtle: fact versus fiction. Fossil Turtle Research 1, 104-111 (2006). Pritchard, P.C.H. Evolution and structure of the turtle shell. In Biology of Turtles (eds. Wyneken, J., Godfrey, M.H. & Bels, V.) 45-83 (CRC Press, Boca Raton, FL, 2008). www.nature.com/nature 5
Rieppel, O. Sauropterygia I: Placodontia, Pachypleurosauria, Nothosauroidea, Pistosauroidea. Encyclopedia of Paleoherpetology, Vol. 12A. Pfeil, Munich (2000). Rieppel, O. The relationships of turtles within amniotes. In Biology of Turtles (eds. Wyneken, J., Godfrey, M.H. & Bels, V.) 345-353 (CRC Press, Boca Raton, FL, 2008). Rieppel, O. & Reisz, R.R. The origin and early evolution of turtles. Annual Review of Ecology and Systematics 30, 1-22 (1999). Scheyer, T.M. Aging the oldest turtles: the placodont affinities of Priscochelys hegnabrunnennsis. Naturwissenschaften, published online 9 May 2008, http://www.springerlink.com/content/d6627l621j82w073/ Sun, Z., Hao, W. & Jiang, D. 2003, Conodont Stratigraphic Evidence for the Age of the Guanling Fauna, Guizhou Province, China. Acta Scientiarum Naturalium Universitatis Pekinensis 39, 118-125. Xu, F, Niu, Z. & Chen, H. 2003, Triassic cephalopods from the Zhuganpo and Xiaowa Formation in Guanling, Guizhou, with a discussion on the age of the Guanling Biota. Geological Bulletin of China 22, 254-265 Zangerl, R. The homology of the shell elements in turtles. Journal of Morphology 194, 383-406 (1939). www.nature.com/nature 6