More on the Origin of Turtles – Lyson et al. 2010

Lyson et al.  (2010 – available online) put together their hypothesis on the origin of turtles. In their abstract, they wrote, “We reanalysed a recent dataset that allied turtles with the lizard–tuatara clade and found that the inclusion of the stem turtle Proganochelys quenstedti  and the ‘parareptile’ Eunotosaurus africanus  results in a single overriding morphological signal, with turtles outside Diapsida.”

Milleretta (RC14 specimen) and the Lyson et al. 2010 tree on the origin of turtles.

Figure 1. Milleretta (RC14 specimen) and the Lyson et al. 2010 tree on the origin of turtles. Note the broad ribs already developing in Milleretta, a sister to Acleistorhinus and Eunotosaurus. On its face this seems like a slam dunk for Eunotosaurus and turtles. However, according to the large reptile tree the origin of turtles parallleled the origin of Eunotosaurus. Missing from the Lyson et al. 2010 analysis is Romeria primus and Stephanospondylus, which are closer to the lineage of turtles. A sister to Romeria primus is the last common ancestor of Eunotosaurus and turtles.

Unfortunately,
Lyson et al. (2010) did not include Romeria primusOrobates (Fig. 2) and Stephanospondylus, three taxa found to be closer to the origin of turtles than Eunotosaurus, a terminal taxon with only one known sister, Acleistorhinus. Unfortunately we have no post-crania for Romeria primus (other than slender manual digits) or Acleistorhinus. That lack of data makes it less obvious how they are related to other taxa, but still the large reptile tree nested them in that fully resolved tree. Stephanospondylus was also the sister to the pareiasaurs, a derived clade previously and correctly associated with turtles, but only at the bases of both clades.

Click to enlarge. These skulls are arranged phylogenetically according to the results recovered from the large reptile tree.

Figure 2. Click to enlarge. These skulls are arranged phylogenetically according to the results recovered from the large reptile tree. This was first published a few days ago.

Would be nice to find the common ancestor of both pareiasaurs and turtles, something a little less turtle-like than Stephanspondylus. For now, Orobates(in yellow, Fig. 2) is the best candidate, and prior to that, Romeria primus (in pink). Orobates and Stephanospondylus are Early Permian. The two turtles are Late Triassic. That gives 60-70 million years to evolve a carapace and plastron, plenty of time for transitional taxa to be discovered in. 

Eunotosaurus

Figure 3. Eunotosaurus, a milleretid not related to turtles, but converged with them in several ways. Actually Eunotosaurus is closer to Acleistorhinus and the Caseasauria, which makes sense if put these two together, like Clark Kent and Superman.

Lyson et al. 2012 did find turtle genes closer to lizard genes, while others did not.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Broom R 1924. On the classification of the reptiles. Bulletin of the American Museum of Natural History 51:39-45.
Geinitz HB and Deichmüller JV 1882. Die Saurier der unteren Dyas von Sachsen. Paleontographica, N. F. 9:1-46.
Gregory WK 1946. Pareiasaurs versus placodonts as near ancestors to turtles. Bulletin of the American Museum of Natural History 86:275-326
Kissel R 2010. Morphology, Phylogeny, and Evolution of Diadectidae (Cotylosauria: Diadectomorpha). Toronto: University of Toronto Press. pp. 185. online pdf
Li C, Wu X-C, Rieppel O, Wang L-T, Zhao L-J 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456: 497-501.
Lyson TR, Bever GS, Bhullar B-AS, Joyce WG and Gauthier JA. 2010. Transitional fossils and the origin of turtles. Biology Letters 2010 6, 830-833 first published online 9 June 2010. doi: 10.1098/rsbl.2010.0371
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. Turtle origins out to sea. Nature 456, 450–451.
Rieppel O and deBraga M 1996. Turtles as diapsid reptiles. Nature 384:453-454.
Rieppel O and Reisz RR 1999. The Origin and Early Evolution of Turtles. Annual Review of Ecology and Systematics 30: 1-22.
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.
Williston SW 1917. The phylogeny and classification of Reptilies. Journal of Geology 28: 41-421.

wiki/Stephanospondylus

They Look Like Turtles. They’re Not Turtles.

Strange Bedfellows
The search for the origin of turtles has produced some odd and divergent nestings, but it’s easy to see the concept in each case. Turtles have a long list of unusual characters led by their carapace and plastron, the “shell” that protects them. They have fewer ribs than most other reptiles. For most researchers the search for turtle sisters has focused on taxa with a carapace and/or fewer and broader ribs.

Proganochelys. Formerly the most primitive turtle.

Figure 1. Proganochelys. One of  the most primitive known turtles.

The Starting Line – The Most Primitive Known Turtles
Of course we have to start with (by universal consensus) the two most primitive turtles, Proganochelys (Baur 1887, Gaffney 1990, Fig. 1, above) and Odontochelys, both from the Late Triassic. In today’s blog we’ll take a look at the “also-rans” and “close but no cigars” that were not related to turtles, yet resembled them by convergence.

Eunotosaurus

Figure 2. Eunotosaurus, a milleretid not related to turtles.

Eunotosaurus
Lyson et al. (2010) added Eunotosaurus africanus (Seeley 1892)  to a tree created by Li et al. (2009) in their earlier study of the basal turtle Odontochelys. Lyson et al. (2010) employed only 30 taxa. Unfortunately they specified “Diadectomorpha” as the outgroup, along with Seymouria. That was an inappropriate decision because Diadectes and Limnoscelis are reptiles nesting deep within the Lepidosauromorpha, as determined by the large study. Lyson et al. (2010) considered Eunotosaurus a turtle sister candidate because it reduced its dorsal rib count to just ten and each one was expanded in width producing a sort of internal carapace. Here, in a larger study that specified Ichthyostega as a basal outgroup Eunotosaurus nested as a sister to Acleistorhinus and Milleretta, which had similarly wide ribs and shared more traits with Eunotosaurus than either did with turtles.

Members of the Placochelyidae

Figure 3. Members of the Placochelyidae, Placochelys, Henodus and Cyamodus in clockwise order.

Placodonts with a Carapace
Members of the Placochelyidae (Fig. 3) were placodonts that developed a turtle-like carapace, but not in the pattern of genuine turtles. Placochelys went so far as to evolve paddles like a sea turtle. Placodonts were slow-moving plant-eaters (or shellfish crushers) that descended from a sister to Palatodonta. de Braga and Rieppel (1997) and Rieppel and Reisz (1999) nested turtles with sauropterygians (which includes placodonts). They considered turtles to be diapsids that had lost their temporal openings. Unfortunately their study also recovered a turtle sisterhood with the Permo/Triassic rib-gliders. So, on the face of it, the likelihood of the slender arboreal gliders as sister taxa to bulky terrestrial turtles and marine herbivores should have raised a red flag.  Here rib gliders and sauropterygians (including placodonts) are not related to each other so turtles cannot nest between them as sister taxa. Too few taxa, once again, is the single source of most of the problems with the studies of de Braga and Rieppel (1997) and Rieppel and Reisz (1999).

Sinosaurosphargis.

Figure 1. Sinosaurosphargis, a shelled sister to Claudiosaurus, not turtles.

A Basal Enaliosaurian
Sinosaurosphargis yunguiensis (Li, Rieppel, Wu, Zhao and Wang 2011) Anisian, Middle Triassic, ~230 mya, ~60 cm in length was originally considered a possible turtle ancestor because the dorsal ribs were broadened to such an extent that the each one touched its neighbors and the torso was covered in bony osteoderms. Here Sinosaurosphargis nested outside the base of the Sauropterygia, as a sister to Claudiosaurus and some distance from the placodonts. Sinosaurosphargis had many more ribs than turtles do, the carapace was not produced the same way as in turtles and the skull was distinct in morphology.

Stephanospondylus
Earlier we looked at the most parsimonious ancestor as determined by the large reptile family treeStephanospondylus did not have a carapace but was a Diadectes-like turtle sister taxon that preceded turtles by 65 million years. So, there was still a big time window in which to find closer turtle ancestors. No carapace or ribs are known for this taxon, but the rest of the anatomy was closer to turtles than any other tested taxon.

Earlier I wrote a short blog on turtle/pterosaur relations, but that was done by eliminating half the taxon list to prove a point and should not be considered the final word due to the mass exclusion experiment. Still, turtles and pterosaurs nested close to each other than to placodonts or dinosaurs.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Baur G 1887. On the phylogenetic arrangement of the Sauropsida: Journal of Morphology, v. 1, n. 1:93-104.
Cisneros JC, Rubidge BS, Mason R and Dube C 2008. Analysis of millerettid parareptile relationships in the light of new material of Broomia perplexa Watson, 1914, from the Permian of South Africa. Journal of Systematic Palaeontology 2008 (6): 453–462. doi:10.1017/S147720190800254X
Cox CB 1969. The problematic Permian reptile Eunotosaurus. Bulletin of the British Museum of Natural History 18: 167–196.
deBraga M and Rieppel 0 1997. Reptile phylogeny and the interrelationships of turtles. Zoological Journal of the Linnean Society 120:281-354.
Gauthier J Kluge AG and Rowe T 1988. Amniote phylogeny and the importance of fossils. Cladistics 4: 105-209
Gaffney ES 1990. The comparative osteology of the Triassic turtle Proganochelys, Bull. Am. Mus. Nat. Hist. 194: 1–263.
Gregory WK 1946. Pareiasaurs versus placodonts as near ancestors to turtles. Bulletin of the American Museum of Natural History 86:275-326
Gow CE 1997. A reassessment of Eunotosaurus africanus Seeley (Amniota: Parareptilia). Palaeontologia Africana, 34:33–42.
Gow CE and de Klerk B 1997. First record of Eunotosaurus (Amniota: Parareptilia) from the Eastern Cape. Palaeontologia Africana, 34: 27–31.
Keyser AW and Gow CE 1981. First complete skull of the Permian reptile
Eunotosaurus africanus Seeley. South African Journal of Science 77: 417–420.
Li C, Rieppel O, Wu X-C, Zhao L-J and Wang LT 2011. A new Triassic marine reptile from southwestern China. Journal of Vertebrate Paleontology 31 (2): 303-312. doi:10.1080/02724634.2011.550368.
Layson TR, Bever GS, Bhullar B-AS, Joyce WG and Gauthier JA 2010. Transitional fossils and the origin of turtles. Biology Letters June 9 2010. doi: 10.1098/rsbl.2010.0371
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: 497-501.
Lyson TR, Bever GS, Bhullar B-AS, Joyce WG, Gauthier JA 2010. Transitional fossils and the origin of turtles. Biology Letters 6:830-833. online PDF
Modesto SP 2000. Eunotosaurus africanus and the Gondwanan ancestry of anapsid reptiles. Palaeontologia Africana, 36:15–20.
Rieppel O and Reisz RR 1999. The Origin and Early Evolution of Turtles. Annual Review of Ecology and Systematics 30: 1-22.
Rubidge BS, Modesto, S, Sidor C and Welman J. 1999. Eunotosaurus africanus from the Ecca–Beaufort contact in Northern Cape Province, South Africa — implications for Karoo Basin development. South African Journal of Science 95: 553–555. online pdf
Watson DMS 1914. Eunotosaurus africanus (Seeley) and the ancestors of the Chelonia, Proceedings of the Zooogical Society of London 11:1011–1020.

What is Eunotosaurus?

Eunotosaurus was a wide-bellied reptile with extremely broad ribs and eight dorsal vertebrae…which is how one could also describe a turtle. Several specimens are known. Smaller than a human hand, some were preserved curled up.

With Turtles. Then Not. Then With Again.
Watson (1914) originally considered Eunotosaurus a turtle ancestor.

Romer (1956) separated Eunotosaurus from turtles, with no other idea how Eunotosaurus nested.

Cox (1969) nested Eunotosaurus with Captorhinus and kin.

Cisneros et al. (2008) nested Eunotosaurus with Milleretta. (Bravo!!)

Currently Lyson et al. (2010) puts Eunotosaurus and turtles together again. Unfortunately the support values were chiefly below 0.66 and too few taxa were used compared to the large study found here. On the plus side, Eunotosaurus did nest with Acleistorhinus and Milleretta in that study.

Eunotosaurus and its sister taxa, Acleistorhinus and Milleretta RC14.

Figure 1. Eunotosaurus and its sister taxa, Acleistorhinus and Milleretta RC14.

The Closest Sister Taxa to Eunotosaurus
Here, in the large study, Acleistorhinus was the closest sister taxon to Eunotosaurus (Figure 1). Unfortunately, only the skull is known. The next closest sister taxon was the RC14 specimen of Milleretta, which shares the expanded ribs that characterize Eunotosaurus. More Eunotosaurus details can be found at reptileevolution.com

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Watson DMS 1914. Eunotosaurus africanus (Seeley) and the ancestors of the Chelonia, Proceedings of the Zooogical Society of London 11:1011–1020.
Cisneros JC, Rubidge BS, Mason R and Dube C 2008. Analysis of millerettid parareptile relationships in the light of new material of Broomia perplexa Watson, 1914, from the Permian of South Africa. Journal of Systematic Palaeontology 2008 (6): 453–462. doi:10.1017/S147720190800254X
Cox CB 1969.
 The problematic Permian reptile Eunotosaurus. Bulletin of the British Museum of Natural History 18: 167–196.
Keyser AW and Gow CE 1981. First complete skull of the Permian reptile
Eunotosaurus africanus Seeley. South African Journal of Science 77: 417–420.
Gow CE 1997. A reassessment of Eunotosaurus africanus Seeley (Amniota: Parareptilia). Palaeontologia Africana, 34:33–42.
Gow CE and de Klerk B 1997. First record of Eunotosaurus (Amniota: Parareptilia) from the Eastern Cape. Palaeontologia Africana, 34: 27–31.
Lyson TR, Bever GS, Bhullar B-AS, Joyce WG and Gauthier JA 2010. Transitional fossils and the origin of turtles. Proceedings of the Royal Society B Available online 9 June 2010: 830. online pdf
Modesto SP 2000. Eunotosaurus africanus and the Gondwanan ancestry of anapsid reptiles. Palaeontologia Africana, 36:15–20.

wiki/Eunotosaurus