Meiolania and the antiquity of turtles

Figure 1. Meiolania is another club-tailed, short-toed turtle like Proganochelys.

Meiolania (Fig. 1, Oligocene to Holocene-only 2000 years ago, Anderson 1925) was a giant horned turtle with a club tail, sort of like the Triassic turtle, Proganochelys (Fig. 2). According to Wikipedia, in Meiolania, “Two large horns faced sideways, giving the skull a total width of 60 centimetres (2.0 ft), and would have prevented the animal fully withdrawing its head into its shell.” The horns appear in a variety of shapes. More recent fossils are found in Australia and New Zealand but Cretaceous specimens are known from Argentina. So, like ankylosaurs, this turtle successfully faced down giant theropod dinosaurs.

Figure 2. Proganochelys and Proterochersis, two Triassic turtles.

Another Triassic turtle,
Proterochersis (Fig. 2), had a shell more like those found in typical turtles. Proterochersis is the earliest known Pleurodire (“side-necked”) turtle.

With this variety in turtles already found in Late Triassic strata, the origin of turtles must be much further back in time. Indeed…

The next prior step in the evolution of turtles
can be found in Stephanospondylus (Fig. 3) of the Early Permian. That gives Permian and Triassic turtles a good 70 million years to evolve and diversify to the grades we find in Proganochelys and Proterochersis. It’s worthwhile to compare these figures to note how far turtles have come and how their basic morphology arose in the Early Permian, fighting off our early ancestors among the ophiacodont and sphenacodont pelycosaurs alongside such as other heavy plant-eaters as Casea and the ancestors of Eunotosaurus.

Figure 3. Click to enlarge. Stephanospondylus parts roughly assembled. Note the origin of the carapace (upper shell) as a broad costal rib. The presence of a plastron (lower shell) is presumed by the distal articular surface of the pubis and the shape of the interclavicle.

Someday
Those tough little Permian and Triassic turtles will be found and they will make big news. Someday Stephanospondylus will be re-examined and appreciated for what it is and that will make big news.

Perhaps now a tip of the hat is due
to a more primitive turtle and Eunotosaurus ancestor, Milleretta (Fig. 4), which survived until the Late Permian, but must have had its origins in the Late Pennsylvanian, millions of years prior to the Early Permian and the appearance of Stephanospondylus. In the Late Pennsylvanian Milleretta was facing down smaller predators, like Palaeothyris and probably Protorothyris among the basal reptiles and Gephyrostegus among the most reptile-like amphibians.

Figure 4. Milleretta, a Late Permian descendant of the Late Pennsylvanian ancestor of turtles, Odontochelys and Eunotosaurus.

I haven’t forgotten Odontochelys
Odontochelys (Fig. 5, Late Triassic) is another descendant of an ancient sister to Milleretta (RC70) but diverged from the ancestors of today’s turtles as we discussed earlier.

Figure 5. Click to enlarge. Odontochelys the quasi-turtle in dorsal, lateral and ventral views. The same for the skull.

So the origin of turtles and the elaborations of their shell was essentially a race against ever larger and more vicious predators, following the Red Queen hypothesis. The ancestors of Meiolania survived until the point that a descendant of Proterothyris (Homo sapiens) finally wiped them out,  a mere 2000 years ago. Happily, a variety of other turtles are still with us.

References
Anderson, C., 1925. Notes on the extinct Chelonian Meiolania, with a record of a new occurrence. Records of the Australian Museum 14(4): 223–242, plates xxx–xl. online pdf
Baur G 1887. On the phylogenetic arrangement of the Sauropsida: Journal of Morphology, v. 1, n. 1:93-104.
Broom R 1924. On the classification of the reptiles. Bulletin of the American Museum of Natural History 51:39-45.
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.
Gregory WK 1946. Pareiasaurs versus placodonts as near ancestors to turtles. Bulletin of the American Museum of Natural History 86:275-326.
Joyce WG, Schoch RR and Lyson TR 2013. The girdles of the oldest fossil turtle, Proterochersis robusta, and the age of the turtle crown. BMC Evolutionary Biology 13: 266. doi:10.1186/1471-2148-13-266 abstract
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, 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/Meiolania 
wiki/Proganochelys
wiki/Stephanospondylus

Eunotosaurus news – svp abstracts 2013

From the abstract:
Bever and Lyson 2013 wrote: “The reemergence of the Middle Permian amniote Eunotosaurus africanus as a potential early stem turtle is based on a number of striking postcranial synapomorphies, many of which are related directly to the evolutionary origin of the iconic turtle shell. Our data reveal a cranial morphology characterized by a large number of plesiomorphic features that suggest Eunotosaurus lies near the base of Panreptilia and outside the early radiation of pandiapsid forms. A good example is the large supratemporal bone that sweeps forward to broadly contact the postorbital – a character essentially unknown in Pandiapsida. The cranial characters of Eunotosaurus that are derived within Panreptilia are variously shared with an interesting taxonomic mix of turtles, parareptiles, and relatively derived diapsids (crownward stem diapsids and crown diapsids). One character that exemplifies this distribution is the slender, vertically oriented quadratojugal. This is a feature present in the early stem turtle Proganochelys quenstedti, a handful of parareptile forms, and as a derived character within Panarchosauria. Almost none of these derived features are shared with those taxa more nearly contemporaneous with Eunotosaurus and that constitute the early portions of the diapsid stem. Eunotosaurus also shares a number of characters with Proganochelys that are not established as present in other parareptiles. Examples include ossification of the anterolateral wall of the braincase and presence of a tall quadrate process of the pterygoid. We articulate and compare the models of cranial evolution as dictated by the currently competing hypotheses for the origin of turtles. The cranial evidence supporting a close relationship between Eunotosaurus and turtles amplifies the apparent conflict between the seemingly plesiomorphic morphology of the turtle stem and the seemingly derived molecular signature of the turtle crown.”

Figure 1. Skull of Eunotosaurus compared to Odontochelys, Proganochelys, Milleretta and Stephanospondylus. The odd bedfellow here in Eunotosaurus, which retains the lateral temporal fenestra of its Milleretta (RC14) and Acleistorhinus (Fig. 2) sister/ancestors.

Earlier we tested Eunotosaurus with 350 reptiles and recovered it as a sister to Acleistorhinus, not turtles. Earlier we tested turtles with 350 reptiles and recovered the stem turtle, Proganochelys with Stephanospondylus far from Eunotosaurus. Even Odontochelys, previously considered a turtle sister, instead nested with the RC 70 specimen of Milleretta.

So that means we have three different convergent origins for turtle-like morphologies. Only one, Stephanospondylus, is the real deal. My guess is Bever and Lyson have not tested it in their “currently competing hypotheses.” They are also stuck with old pseudo clades, like Parareptilia, that lose their utility when the gamut of included taxa is increased here.

Figure 2. Acleistorhinus is a sister to Milleretta (RC14) and Eunotosaurus. Lanthanosuchus, previously considered close to Acleistorhinus, is more closely related to Romeriscus and Macroleter, all three of the flathead variety.

As you can see from the above illustrations, Acleistorhinus is the closest sister to Eunotosaurus. And Stephanospondylus is the closest known sister to turtles. More details are available by clicking the taxon links above.

References
Bever G and Lyson T 2013. Cranial evolution and the origin of turtles: insights from Eunotosaurus africanus. Journal of Vertebrate Paleontology abstracts 2013. 

Thoracic transverse processes – here and there

In reptiles sometimes the dorsal (thoracic) vertebrae develop elongate transverse processes (Fig. 1). The phylogenetic pattern of these appearances is today’s topic, inspired by Hirasawa 2013.

Note (Fig. 1) that the turtle-like enaliosaur, Sinosaurophargis has elongate thoracic transverse processes. Turtles and near-turtles, like Odontochelys, don’t. So why did Hirasawa et al. (2013) add Sinosaurosphargis to their turtle family tree? Were they influenced by the convergent carapace?

The large reptile tree found the two clades (turtles and saurosphargids) were not related. Turtles nested with the new lepidosauromorphs, while saurosphargids nested with the new archosauromorphs.

Figure 1. from Hirasawa et al. 2013, pink arrow points to elongate transverse processes on Sinosaurosphargis. These are not present on Odontochelys and turtles. We’ll look at where in the tree such processes do appear  by convergence. 

The appearance of thoracic transverse processes within the Reptilia
You’ll recall that reptiles are essentially diphyletic. We’ll start with one of these clades, then look at the other in the large reptile tree.

The pattern of appearance within the new Lepidosauromorpha
The first appearance of transverse processes in the new Lepidosauromorpha is at the Kuehneosauridae, the gliding reptiles of the Permian to Cretaceous.

The only other clade is the Fenestrasauria (including the Pterosauria) of the Triassic to Cretaceous.

So, no turtles or near-turtles have elongate transverse processes.

The pattern of appearance within the new Archosauromorpha
The entire Synapsida develop elongate transverse processes in the new Archosauromorpha.

The next appearance includes the turtle-like basal enaliosaurs, Sinosaurosphargis (Fig. 1) + Largocephalosaurus.

Eusaurosphargis alone among thalattosaurs develops elongate transverse processes. It also has a wide, flattened torso, but gracile ribs.

Placodonts have elongate transverse processes. So do plesiosaurs, but not nothosaurs or pachypleurosaurs.

The pararchosauriforms from Doswellia to Tropidosuchus all have elongate transverse processes.  (Does Lagerpeton follow this pattern?)

Basal euarchosauriforms up to and including rauisuchids do not have elongate transverse processes. Derived rauisuchia from Yarasuchus and Ticinosuchus through all crocs and dinos (including birds and poposaurs) do have elongate dorsal transverse processes.

Pattern?
Wide flat taxa tend to have elongate transverse processes, whether they are trying to increase their width to glide or to flatten out on the ground or underwater. Even so, many flattened taxa do not have elongate transverse processes.

The stiffening of the torso (less undulating) appears to be the second reason, seen in synapsids, fenestrasaurs, pararchosauriforms and derived rauisuchians.

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

Lee 1993 – An Important Contribution to Turtle Origins

Earlier we looked at several convergent turtle-like taxa. Today we’ll take a good look at the pareiasaurs, the second* closest taxon to the turtles themselves.

The origin of turtles
is one of the most hotly debated topics in paleontology. Unique among living amniotes, turtles have a carapace, plastron and a shoulder girdle within the rib cage. Some DNA studies point to an archosaur link. Other studies link turtles to lizards. Only the large reptile tree looked at over 335 possible nesting sites for turtles and came up with one.

Dr. Michael S. Y. Lee (1993) provided the best published morphological report on turtle origins to date. This paper precedes the discovery of Odontochelys (Li et al. 2008), overlooks Stephanospondylus (Geinitz and Deichmuller 1882) and nests turtles with pareiasaurs like Deltavjatia (Hartmann-Weinberg 1937).

Figure 1. The pareiasaur Deltavjatia identifying turtle traits: A2 – Foramen palatinum medially located (similar to the suborbital fenestra). A8 – Supraoccipital forms a long, high, narrow and median ridge sutured to the skull roof along its entire length. A12 – Scapula with acromion process on the anterior margin. A13 – Humerus with ectepicondylar foramen. B1 – (Fig. 1) Twenty or fewer presacral vertebrae. B2 – Tall and narrow scapula (4x higher than wide). B3 – Shoulder glenoid not screw-shaped, but bipartite. B4 – Scapula oriented anterodorsally, not horizontally. B8 – Thick dermal armor over the dorsal region.

In Lee (1993) pareiasaurs were found to share 16 derived traits with turtles. These traits are identified with an “A“.

Cranial traits synapomorphies:
A1 – (Fig. 2) Choana (internal nares) located far medially.
A2 – (Figs. 1,2) Foramen palatinum medially located (similar to the suborbital fenestra).
A3 – (Fig. 2) Massive horizontal paroccipital process sutured to squamosal.
A4 – (Fig. 2) Long lateral flange of the exoccipital on the posterior face of the paroccipital process.
A5 – (Fig. 2) Basisphenoid and basioccipital ossified together.
A6 – (Fig. 2) Ossified medial wall of prootic.
A7 – (Fig. 2) Transverse flange of pterygoid reduced and forwardly directed.
A8 – (Fig. 1`) Supraoccipital forms a long, high, narrow and median ridge sutured to the skull roof along its entire length.
A9 – The entire palate is raised well above the ventral margin of the maxilla.

Figure 2. More turtle traits in pareiasaurs. A1 – Choana located medially. A2 -Foramen palatinum medially located. A3 – Massive horizontal paroccipital process sutured to squamosal. A4 – Long lateral flange of the exoccipital on the posterior face of the paroccipital process. A5 – Basisphenoid and basioccipital ossified together. A6 – Ossified medial wall of prootic. A7 – Transverse flange of pterygoid reduced and forwardly directed. A9 – The entire palate is raised well above the ventral margin of the maxilla.

Postcranial Trait Synapomorphies
A10 – (Fig. 3) Prominent lateral projections on at least the first 14 caudal vertebrae.
A11 – (Fig. 3) Chevrons not wedged between adjacent centra.
A12 – (Figs. 1, 3) Scapula with acromion process on the anterior margin
A13 – (Fig. 1) Humerus with ectepicondylar foramen.
A14 – (Fig. 3) Femur with a major trochanteron the posterior margin.
A15 – (Fig. 3) Reduced pedal digit 5.
A16 – Prominent dorsal buttress, V-shaped in ventral view, overhanging the acetabulum.

Figure 3. Postcranial turtle traits in pareiasaurs. A10 – Prominent lateral projections on at least the first 14 caudal vertebrae. A11 – Chevrons not wedged between adjacent centra. A12 – Scapula with acromion process on the anterior margin. A14 – Femur with a major trochanteron the posterior margin. A15 – Reduced pedal digit 5.

Sclerosaurus
Nine more traits are shared by Proganochelys, pareiasaurs and Sclerosaurus, the smaller, flatter, pareiasaur sister. These are identified with a “B” by Lee (1993).

B1 – (Fig. 1) Twenty or fewer presacral vertebrae.
B2 – (Figs. 1, 3) Tall and narrow scapula (4x higher than wide).
B3 – (Figs. 1, 3) Shoulder glenoid not screw-shaped, but bipartite.
B4 – (Figs, 1-3) Scapula oriented anterodorsally, not horizontally.
B5 – Reduced manual phalangeal formula (23332)
B6 – (Fig. 3) Astragalus and calcaneum fused
B7 – (Fig. 3) Reduced pedal phalangeal formula (23343)
B8 – (Fig. 1) Thick dermal armor over the dorsal region.
B9 – Loss of gastralia.

The large reptile tree found Sclerosaurus to be a derived pareiasaur, not closer to turtles. Chronologically Stephanospondylus preceded turtles and Sclerosaurus by 70 million years. Stephanspondylus preceded pareiasaurus by 35 million years, plenty of time for these radiations to occur. Look for primitive turtles in the mid to late Permian, concurrent with pareiasaurs.

But wait, there’s more…
The large reptile tree used only a few of the above traits yet to likewise nest turtles with pareiasaurs and Sclerosaurus. Stephanospondylus does not preserve any palate, tail, manus femur, pes or armor data.

The scapula question
Lee notes that pareiasaurs and Sclerosaurus possess 5 cervicals and 14-15 dorsals for a total of 19 to 20. Turtles possess 8 cervicals and 10 dorsals, meaning that 3 turtle cervicals are former dorsals. This change was accompanied by a posterior shift of the pectoral girdle (Watson 1914) that is recapitulated during turtle ontogeny (embryogenesis).

All known pareiasaurs are too pareiasaur-y to be ancestral to turtles
*Stephanospondylus is a key taxon linking diadectids to pareiasaurs and turtles that avoids being to “pareiasaur-y.” No known archosaur shares so many turtle traits. No known sauropterygian comes close either. Out of 335+ taxa, Stephanospondylus remains the best candidate I’ve found. But, sans that taxon, turtles would nest just outside the Pareiasauria.

Hats off to Dr. Lee for doing a great job.

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
Geinitz HB and Deichmüller JV 1882. Die Saurier der unteren Dyas von Sachsen. Paleontographica, N. F. 9:1-46.
Hartmann-Weinberg AP 1933. Evolution der Pareiasauriden: Trudy Palaeontological institute Academe Nauk, SSSR, 1933, n. 3, p. 1-66.
Lee MSY 1993. The Origin of the Turtle Body Plan: Bridging a Famous Morphological Gap. Science 264:1716-17-1719.
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.
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.
Watson DMS 1914. Eunotosaurus africanus Seeley and the ancestors of the Chelonia. Proceedings of the Zoological Society of London 11:1011.

Palaos discussion

Eight convergent turtle-like morphologies

Turtles have an unusual morphology.
So unusual are turtles that most paletonotolgists are still wondering from whence they came. Various professors use fossils to support their hypotheses. Othere use DNA. All these attempts result in different answers. Even the genetic story has flip-flopped from archosaurs to lepidosaurs and back again.

The problem is turtles (Figs. 1,2) are different from all living animals and distinct from most prehistoric ones. Their roots are very deep. Earlier we looked at taxa that looked like turtles, but were not turtles. Here we’ll expand that list.

What are turtles?
Phylogenetically what we’re looking for is the reptile most like a turtle that is not yet a turtle. We know of several turtle-like reptiles (see below), but none share a turtle’s basic anatomy. They all developed their protective shells via convergence.

Genes
A recent (May 15, 2012) online story here reports from Crawford et al. (2012), “Scientists lift lid on turtle evolution. Anatomy and fossil studies of turtles and their reptilian relatives generally place the shelled creatures in the family of lepidosaurs — snakes, lizards and tuataras (rare lizard-like animals). Genetic studies, however, say they have more in common with crocodiles and birds.”

Of course,
if turtled did descend from archosaurs and their kin, then we have to look for the closest relatives of turtles in the new Archosauromorpha. Trouble is, given the widest gamut of possibilities yet offered, turtles nest in the other lineage, of lizards and their kin, not with archosaurs. Other respected genetic studies, like Lyson et al. (2012), report turtles are genetically closer to lizards.

So how do we solve this problem?
We can’t. All three sides have their proof.

Of course, someday you’ll have to find a non-turtle that looks like a turtle, and that’s phylogeny and morphology. So, here we’re going to look at seven distinct types of reptiles (including mammals) that had a turtle-like morphology. We’ll start with turtles themselves.

Figure 1. Proganochelys from the Late Triassic. Formerly the most primitive turtle.

Figure 2. Odontochelys, also from the Late Triassic, the new most primitive turtle. It has teeth. The carapace is missing. Lost or not yet developed has not been determined yet.

Figure 3. Stephanospondylus from Romer (1925). According to the results of the large reptile tree, this is the most turtle-like non-turtle yet discovered. And yet, among all these taxa, it’s the only one without a shell or scutes (that I know of). Chronologically Stephanospondylus precedes the Odontochelys by 70 million years, plenty of time to iron out the differences and plenty of time to find a transitional taxon or ten, seven million years apart from each other someday. No carapace or plastron was preserved with Stephanospondylus.

1. Turtles themselves
Derived from Stephanospondylus, turtles like Odontochelys and Proganochelys have a plastron, but only Proganochelys has a carapace. Thus, Odontochelys was analogous to a “soft-shelled” turtle, but not directly related. Turtles have fewer than ten dorsal ribs and have no temporal fenestrae. Stephanospondylus is a little-studied diadectomorph close to pareiasaurs that happens to share more traits with turtles than any other studied taxon. Unfortunately, it is incompletely known and crushed. We studied Stephanospondylus earlier here. I hope other paleontologists will begin to consider this long neglected taxon in their turtle studies, at least to test the large reptile tree results. In order to do so, they will also have to recognize the reptile traits of diadectomorphs. Unfortunately at present diadectomorphs are widely considered to be non-amniotes close to basal amniotes.

Figure 2. Cyamodus, a sharp-snouted shelled placodont.

2. Cyamodontids
Derived from Palatodonta, cyamodontids like Cyamodus and Placochelys have a carapace and a second smaller one over the hips. Huge upper temperal fenestra and flat-pebble-like teeth differentiate this placoderm from turtles.

Figure 3. Henodus, a broad-snout shelled placodont

3. Henodus
Derived from a sister to Placodus, Henodus is another placodont with an independently evolved wrap-around carapace and tiny legs projecting out of anterior and posterior openings. Tiny upper temporal fenestra and a broad rostrum differentiated this taxon from turtles and cyamodontids.

Figure 5. Sinosaurosphargis. Click for more information. Not sure about the anterior extent of the maxilla, here shown two ways. Ribs and gastralia like these are not known in Omphalosaurus, which has more plesiomorphic and typical looking ribs and gastralia.

4. Sinosaurosphargis
Derived from Claudiosaurus, Sinosaurosphargis and Largocephalosaurus have a carapace covering dozens of wide flat ribs and gastralia. The nostrils are located midway between the long snout tip and orbit.

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

5. Eunotosaurus
Derived from Acleistorhinus, Eunotosaurus has nine expanded ribs, like turtles, but no true carapace or plastron. Lateral temporal fenestra are present. The tail is exceptionally long.

Figure 7. Ankylosaurus, dorsal view. This early image was made prior to the discovery of tail clubs in ankylosaurs, but reflects the distribution of osteoderms over the bak.

6. Ankylosaurs
Derived from basal ornithischian dinosaurs like Scelidosaurus, ankylosaurs like Ankylosaurus, had a carapace made of osteoderms.

Figure 8 Stagonlepis, an aetosaur derived from rauisuchians

7. Aetosaurs
Derived from odd rauisuchians like Ticinosuchus, aetosaurs like Stagonlepis (Fig. 8) also had a carapace made of osteoderms.

Figure 10. Glyptodon, a glyptodont/edendate/mammal.

8. Glyptodonts and Armadillos
Derived from armadillo-like ancestors, glyptodonts like Glyptodon, had a carapace made of hexagonal scutes, otherwise known as bony skin scales called osteoderms.

I’m not including Jaxtasuchus, an armored protorosaur, which we looked at earlier. It could be number nine, but it’s getting longer and thus less turtle-like.

So, turtle-like anatomies are fairly common in the prehistoric past. Now, not so much, but turtles themselves display a wide variety of types and sizes and niches. Most paleontologists understand that these taxa are all distinct from turtles. However, when some of these taxa are included in phylogenetic analyses without also including Stephanospondylus, pareiasaurs and diadectids, then turtles tend to be attracted to these shelled wonders and thus skew the results toward placodonts or eunotosaurs (Lyson et al. 2010).

Just want to give the rightful ancestors their due. The strength of the large reptile lies in its ability to differentiate the true ancestors of turtles from the convergent pretenders.

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
Crawford NG, Faircloth BC, McCormack JE, Brumfield RT, Winker and Glenn TC 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biology Letters, 2012; DOI: 10.1098/rsbl.2012.0331.
Lyson TR, Bever GS, Bhullar B-AS, Joyce WG and Gauthier JA 2010. Transitional fossils and the origin of turtles. Biology Letters 6 (6): 830–833. 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.
Rieppel O and DeBraga M. 1996. Turtles as diapsid reptiles. Nature 384 (6608): 453–5. doi:10.1038/384453a0.

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.”

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 primus, Orobates (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.

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. 

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

More on the origin of turtles

Earlier we looked at the origin of turtles.

This blogpost has been essentially deleted after the addition of several basal taxa to the large reptile tree. Click here for updates added Feb. 2016.

References
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.
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

wiki/Odontochelys

Carroll and Rieppel on the Origin of Turtles

Two new papers on turtle origins open this subject again.

Carroll (2012) examines a number of possibilities then arrives at Eunotosaurus (Figs. 1, 3) as the best of a bad bunch.

Rieppel (2012) restudies Odontochelys the most primitive known turtle.

I haven’t read either paper, only the abstracts. Both are on request. If anyone has these, I would certainly appreciate a copy.

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

From Carroll (2012): “The unquestioned unity of the Chelonia provides a necessary basis for establishing their interrelationships and determining the evolutionary history within the group. On the other hand, the host of uniquely derived features of the oldest known turtles make it extremely difficult to establish their ancestry among more primitive amniotes. This is illustrated by the great diversity of taxa that continue to be proposed as putative sister-taxa of turtles without general acceptance of any. Nearly every major clade of early amniotes from the late Paleozoic and early Mesozoic has been proposed as a possible sister-taxon of turtles, from synapsids to anapsids and diapsids, including pelycosaurs, captorhinomorphs, procolophonids, pareiasaurs, aquatic placodonts and crocodiles, but none possess derived characters that could be synapomorphic with the unique skeletal structure and patterns of development of the chelonian skull, carapace or plastron, which had reached an essentially modern configuration by the Late Triassic. Numerous molecular biologists have attempted to establish the closest sister-group of turtles through analyses of a host of living species, but there is no way for them to preclude turtles from
having evolved from one or another of the Paleozoic or early Mesozoic clades that have become extinct without leaving any other living descendants. On the other hand, recent studies of the genetic and molecular aspects of the development of the carapace and plastron imply unique patterns of evolutionary change that cannot be recognized in any of the other amniote lineages, living or dead. This, together with the retention of a skull without temporal fenestration implies a very early divergence from a lineage that probably retained an anapsid skull configuration. This problem may be resolved by more detailed study of the enigmatic genus Eunotosaurus, from the Late Permian of South Africa.”

The large reptile tree found pterosaurs to be the closest sister taxa of turtles (!!–huh-huh-huh- —  but only in the absence of all other new Lepidosauromorpha!!!).

By including all 315 reptile taxa (half of these are lepidosauromorphs), a more parsimonious and complete tree links the overlooked diadectid, Stephanospondylus (Fig. 2) to turtles. Increasingly distant relatives include the basal pareiasaur Arganaceras, Diadectes and Orobates.

Figure 2. From left to right the skulls of Stephanospondylus, Odontochelys and Proganochelys demonstrating tooth loss and other skull traits.

Note that Carroll (2012) did not list any diadectids. Unfortunately, it has been a common oversight in reptile phylogenetic studies to not list the most closely related taxa. Eunotosaurus had a lateral temporal fenestra and nested with millerettids (Fig. 3) including Acleistorhinus. The strength of the large reptile tree is its ability to avoid nesting convergent taxa together (contra the untested worries of several critics).

Figure 3. Eunotosaurus and its sister taxa, Acleistorhinus and Milleretta RC14.

Earlier we talked about the origin of turtles here and here as recovered by the large reptile tree. It’s an interesting tale that has yet to make the rounds of academic publication.

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
Carroll  RL 2012. Problems of the Ancestry of Turtles. Morphology and Evolution of Turtles. Part 2, 19-36. DOI: 10.1007/978-94-007-4309-0_3
Rieppel O 2012. The Evolution of the Turtle Shell. Morphology and Evolution of Turtles. Part 2, 51-61. DOI: 10.1007/978-94-007-4309-0_5

Turtle molecules link them to archosaurs??

A new paper (Crawford et al. 2012) reports that turtle molecules link them to archosaurs, not lepidosaurs.

Here’s the abstract
We present the first genomic-scale analysis addressing the phylogenetic position of turtles, using over 1000 loci from representatives of all major reptile lineages including tuatara. Previously, studies of morphological traits positioned turtles either at the base of the reptile tree or with lizards, snakes and tuatara (lepidosaurs), whereas molecular analyses typically allied turtles with crocodiles and birds (archosaurs). A recent analysis of shared microRNA families found that turtles are more closely related to lepidosaurs. To test this hypothesis with data from many single-copy nuclear loci dispersed throughout the genome, we used sequence capture, high-throughput sequencing and published genomes to obtain sequences from 1145 ultraconserved elements (UCEs) and their variable flanking DNA. The resulting phylogeny provides overwhelming support for the hypothesis that turtles evolved from a common ancestor of birds and crocodilians, rejecting the hypothesized relationship between turtles and lepidosaurs.

Ahh, but which archosaurs?
That’s what molecules will never tell you.

At the end we can only confirm with fossil bones
We’ve already uncovered a most parsimonious nesting and a series of gradually accumulating turtle traits in a lineage within the lepidosauromorpha. So if molecules tell a different tale, then someone’s got some ‘splaining to do. Not sure why the molecules would take us one way while the bones take us another.

Turtles are weird.

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
Crawford NG, Faircloth BC, McCormack JE, Brumfield RT, Winker K, and Glenn TC 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biology Letters (advance online publication) doi:10.1098/rsbl.2012.0331   online

Tooth Loss in Turtles

An online paper by Davit-Béal, Tucker and Sire (2009) examined tooth loss in several tetrapod clades. They mentioned tooth loss in “toads in Lissamphibia, turtles and birds in Sauropsida, and baleen whales, pangolins, anteaters, sloths, armadillos and aardvark in Mammalia.” There were other extinct forms that also lost all* their teeth, including pterosaurs, certain poposaurs and other dinosaurs (ornithomimosaurs). I want to focus on turtles today.

Origins Questioned
Davit-Béal et al. (2009) wrote: “The origin of turtles from ancestral sauropsids is still unclear and largely debated. Molecular data are partially congruent with morphological characters supporting diapsid rather than anapsid turtle relationships [Rieppel & deBraga, 1996; deBraga & Rieppel, 1997; see Laurin & Reisz, 1995 and Lee, 1997 for Parareptilia (anapsid) turtle relationships]. However, the molecular data conflict with palaeontological data as to where exactly turtles fit within diapsids (Rieppel, 1999). Phylogenetic studies either place turtles close to the lepidosaumorphs (tuatara, snakes and lizards) (e.g.Hill, 2005) or close to the archosauromorphs (crocodiles and birds) (e.g. Hedges & Poling, 1999; Iwabe et al. 2005). The turtle ancestor diverged from the other diapsids between 285 and 270 Ma (McGeoch & Gatherer, 2005) but its origin remains a mystery. The most ancient and well-known turtle is Proganochelys quenstedti (late Triassic, 220 Ma).”

Figure 1. Clicking will NOT enlarge image. Toothlessness in turtles according to Davit-Béal et al. (2009). Click to enlarge. Green lines are turtles with palatal teeth. Red lines are turtles without any teeth.

Written Just Before Odontochelys
Timing is everything and the Davit-Béal paper was likely “in press” when the Odontochelys (225 mya) paper was published (Li et al. 2008). Odontochelys is the only known primitive turtle with teeth on the rims of its jaws. Proganochelys and several other early turtles retained palatal teeth. Here the primitive diadectomorph Stephanospondylus (290 mya) is in the clade of turtles, prior to the development of the carapace and plastron 75 million years before turtles with shells.

Figure 2. From left to right the skulls of Stephanospondylus, Odontochelys and Proganochelys demonstrating tooth loss and other skull traits.

Notes from Davit-Béal (2009) 
Davit-Béal et al. (2009) reported, “P. quenstedti was roughly similar to the species that live today, except for, among other characters, the presence of several rows of conical teeth on the vomers, palatines and pterygoids (Fig. 6D), which make it unique among Testudinata as the other ancient turtles lack these teeth (Joyce, 2007). The maxilla, pre-maxilla and dentary are edentulous but the pre-maxillary has tooth vestiges (Kordikova, 2002). Although the common ancestor of all living turtles was aquatic, the earliest turtles clearly lived in a terrestrial environment (Joyce & Gauthier, 2004; Scheyer & Sander, 2007).  As suggested for birds, the presence of a keratinized beak that was efficient for food uptake probably relaxed the functional pressure on teeth, which were probably lost through a similar process to that described in birds (see above). In the turtle’s ancestor, as in the bird’s ancestor, the beak minimized the negative consequences of tooth loss. In turtles, teeth were retained on the palate longer than in jaws. Teeth were lost in the vomers and palatines first, then later on the pterygoids.”

Stepping Back in Time and Phylogeny
The present tree indicates that a sister to Orobates and Diadectes preceded Stephanospondylus and Arganaceras was a basal pareiasaur sister. These taxa are widely considered to be herbivores. The 16 teeth in the left premaxilla (4) and maxilla (12) of Orobates were larger anteriorly and the tooth row ended below the mid orbit. The 15 to 21+ teeth in the left premaxilla and maxilla of Diadectes followed these patterns, but were smaller overall. The sisters Oradectes and Silvadectes were not much different.

Stephanospondylus Teeth
Romer (1925) illustrated 27 teeth in the premaxilla (3) and maxilla (24) of Stephanospondylus extending posteriorly beyond the mid point of the orbit. Each tooth had a smaller diameter but a longer length.

Odontochelys Teeth
In the one and only known toothed turtle (Li et al. 2009) 6 teeth were in the premaxilla and 18 in the maxilla. Distinct from Stephanospondylus, the premaxillary teeth were smaller than the maxillary teeth. Instead of four, there were six premaxillary teeth. The maxillary teeth started off small anteriorly, but were larger posteriorly and extended behind the orbit. As in Stephanospondylus the first maxillary tooth was slightly larger than the others.

Summary
Smaller and an increased number of teeth often precede the complete loss of teeth, as seen here in turtles. Herbivores often lose their teeth, as seen here in turtles. Turtle ancestors provide one of the few examples of herbivores that became insectivores and piscivores. Perhaps they were always omnivores. Like birds, early turtles developed a shearing keratinous beak, providing a substitute for teeth. They have no other similarities that I know of and must have developed beaks for distinct reasons.

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.
Davit-Béal T, Tucker AS and Sire J-Y 2009. Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations. Journal of Anatomy 2009 April; 214(4): 477–501. doi:  10.1111/j.1469-7580.2009.01060.x
Gaffney ES 1990. The comparative osteology of the Triassic turtle Proganochelys, Bull. Am. Mus. Nat. Hist. 194: 1–263.
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.
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/Proganochelys
wiki/Odontochelys