Turtles as they might have been
What are turtles, exactly?
Since the dawn of the cladistic age, phylogenetic systematists have grappled with the question of where turtles belong on the amniote tree. The figure at right is a simplified picture of the options that have been mooted. It is hard to identify shared similarity with creatures who are jus so different - a diabolically intractable problem. And yet, the last five years have seen a real breakthrough. As we review the history, we should be mindful of just how difficult it is to zero in on an answer when you lack key information.
The Early Permian captorhinid Eocaptorhinus laticeps
(Late Carboniferous - Late Permian) Our starting point, and Turtle aficionado Eugene Gaffney's 1988 choice, for sister taxon of Testudinata. Captorhinids (basal sauropsids) are characterized by adaptations to a strong, slow bite with trends toward rounded crushing teeth in multiple tooth-rows. Including Eocaptorhinus (right) but also larger forms such as Labidosaurikos (~1.5 m).
Compared to diapsids, captorhinids seem primitive, having:
- Anapsid skulls with fully-covered skull roofs
- No suggestion of an impedance-matching ear.
Gaffney, however, was intrigued by the fact that both they and turtles, in common, lacked several bones of the skull roof typically found in other sauropsids.
Parareptilia:Parareptilia: (Permian - Triassic (or possibly Recent)) Up until now, we have omitted this large group of fossil sauropsids, although it contains a number of distinct obscure fossil groups. Our reasons for covering them here will become apparent soon. Most parareptiles retain either the anapsid condition of the skull or the synapsid condition. One pattern they don't show is the diapsid pattern. Most cladistic analyses find them to be basal sauropsids, outside of Diapsid, yet Ford and Benson, 2019 find them to nest within Diapsid, as basal members! At various points, turtles have been proposed to nest within Parareptilia.
The procolophonoid Owenetta from the U. C. Berkeley History of Life.
- Jaw articulation well anterior to occipital condyle (a condition shared with turtles.)
- Caniniform teeth (synapomorphy of Amniota) are lost
- Posterior emargination of temporal region, creating an otic notch supported by the quadrate, squamosal, and quadratojugal. (A separate derivation of the impedance-matching ear from that of Temnospondyli, Synapsida, or Sauria.)
Sclerosaurus armatus by D. Bogdanov from Wikipedia
- Proportions: Generally small, squat, robust reptiles, some superficially resembling horned lizards.
- Teeth: Blunt and strong, presumably for processing plant material.
- Skull shape reveals two derived features:
- Quadrate embayed posteriorly to support tympanum.
- Orbits are enlarged posteriorly, possibly functionally equivalent to temporal fenestrae in other amniotes.
- Armor: Some members had dermal scutes in skin. (E.G. Sclerosaurus - right)
But are they pantestudines? Procolophonoids got the spotlight by Reisz and Laurin 1991, who proposed that they were closely related to Pantestudines.
The pareiasaur Scutosaurus inevitably serving as gorgonopsian-food by D. Bogdanov from Wikipedia
- Proportions: Medium to large herbivorous reptiles. Short, deep and wide bodies, presumably with large digestive systems. Probably similar ecologically and metabolically to living giant tortoises.
- Skull: Short and wide, characterized by flaring armored cheeks, bumps and horns. E.G.: Bunostegos. There is no temporal fenestration or anything analogous to it.
- Teeth: Teeth are leaf-shaped, similar to those of large herbivorous iguanas.
- Armor: Pareiasaurs have extensive dermal armor. In some, the armor is interlocking.
But are they pantestudines? Michael Lee, 1993 considered features of their pectoral girdle, and axial skeleton to be strongly suggestive of a connection. Their heavy armor of scutes added color to the argument. Indeed, Lee 1993 considered it likely that that turtles were actually nested within Pareiasauria.
The placodont Henodus chelyops
- the armor is made of dermal scutes that do no fuse with the ribs
- and separate thoracic and pelvic shields are often present.
The turtle as archosaur from The Australian, 8/22/2013
All of the foregoing took place in the near absence of informative fossils of anything more basal than Proganochelys. By 2005, three general positions had crystallized:
- Turtles belong to Parareptilia (Based on morphology)
- Turtles belong to Diapsida (Based on morphology)
- Turtles belong no only to Diapsida, but specifically to Archosauria (Based on DNA)
Why is this so hard?
One issue is long branch attraction, a hazard of phylogenetic systematics.
Imagine a polite tree, in which every monophyletic group is diagnosed by a snapomorphy. Such a phylogeny should be easy to reconstruct using or TnT. The greater the number of characters changing, the easier the reconstruction.
Now imagine a tree with relatively few branches that bifurcate early on then follow independent, non-bifurcating courses of evolution. Imagine a character flipping back and forth between two states. This time, when we attempt to reconstruct the phylogeny, we are in trouble. The character state changes on our long lonely branches do not diagnose new groups. Instead, they simply conceal the lineage's state when it first speciated. When we perform an analyses of these characters, we are analyzing noise more than signal. As a result, we are likely to be positively misled by the analysis because TNT might construe random character changes on these long branches as synapomorphies. This is the long branch attraction problem.
Indeed, there are some hypothetical tree shapes in which the more characters you use, the more likely you are to be misled. This region of "tree-space" called the Felsenstein zone, after its discoverer, Joe Felsenstein.
Conditions where long branch attraction is a danger:
- Very rapidly evolving characters.
- Very old branches with poor fossil record. This points out the real utility of fossils in phylogenetic analysis. Sure they are incomplete and, at best, sample only the anatomy of hard parts of the body, but they are real information from earlier stages of evolution that serve to break-up long branches.
Archaeopterys lithographics, transitional fossil and cultural icon.
Then the new fossils appeared
The last twelve yearsLi et al., 2008, the Late Triassic Odontochelys of China was the most anatomically primitive turtle known. Indeed, it definitely lacks two fundamental turtle features:
- The toothless mouth. Odontochelys has typical simple teeth.
- A carapace.
Odontochelys appears to support the diapsid turtle hypothesis:
- Its depositional environment and limb shape indicates that it was aquatic or semi-aquatic. (It certainly lived close enough to the water for its body to get washed in).
- It's ribs are expanded into paddle-shapes.
- It has no pareiasaur-like scutes.
Eunotosaurus africanus from SciNews
It was not studied cladistically until the 21st century when Lyson et al., 2010 re-ran the Rieppel and deBraga 1996 matrix adding Eunotosaurus and Proganochelys. The result: Testudata popped out of Diapsida.
- Werneburg and Sanchez-Villagra, 2009: Compiled an amniote phylogeny based on developmental timing features of organs and determined based on it that turtles are outside of Diapsida. (Of course only living taxa could be considered in this way.)
- Werneburg et. al, 2013 examined the development of the turtle neck, identifying embryonic intercentra and ribs that become coossified into cervical vertebrae. Among diapsids, intercentra are greatly reduced, so their presence among turtles appears to argue for a non-diapsid origin.
- The neural and costal plates of the turtle shell are associated with vertebrae and ribs, respectively. Lyson et al., 2013 considered the homology of the enigmatic nuchal plate (right) , which has no vertebral component, and find it to be homologous to the cleithra of other amniotes. Recall that the cleithrum was the major bone of the pectoral girdle in fish-like sarcopterygians, reduced in amniotes, and lost in Sauria. The presence of the cleithrum in turtles, places them outside of Sauria. Sorry, archosaurs!
2015 - Summer of Revelation:
When I taught HONR219D in 2014, the accumulating morphological and developmental data seemed to support the parareptilian hypothesis of turtle origins. Then came an interesting summer:
Pappochelys rosinae from Carnivora
- Its ribs are expanded but there are no dermal scutes associated.
- Its gastralia are very robust but not developed into a plastron.
But its remarkable feature is its diapsid skull, that with its ventrally open infratemporal fenestra resembles that of a derived stem saurian. It appears that turtles are, in fact, some kind of diapsid.
But what about Eunotosaurus? It has an anapsid skull, right?
Eunotosaurus skull with supratemporal digitally removed from Bever et al., 2015.
Why would Eunotosaurus do this?
- The strengthening of the skull is common in fossorial animals. Seeing this in Eunotosaurus is consilient with Lyson et al.'s, 2016 argument for fossoriality.
And what does this tell us about the importance of fenestration patterns as "key characters" in taxonomy? :-(
So what are they?OK, I was wrong. Turtles belong in Diapsida. But what about the molecular evidence? Do we just shrug our shoulders and admit that turtles belong in Archosauria? Not yet! The scapula of Pappochelys is informally reported to have:
- a facet for the cleithrum
- no descending flanges of the parietal
That indicates that although they are diapsids, they are outside of Sauria.Of course, no morphological data really refutes the molecular data that suggest that turtles are archosaurs. Indeed, it is difficult to compare these data directly. We await further revelation.