"God's noblest creation"

John Merck

And now, a problem....

Testudo, Malaclemys terrapin, the diamond-back terrapin
We have failed to address one sauropsid group that is dear to our institutional heart. We have saved Testudinata - turtles - for last because they have long represented the greatest challenge of any enigmatic vertebrate to phylogenetic systematics, despite their being very easy to recognize.

Stupendemys geographicus, the largest turtle ever


(Permian - Quaternary) The total group containing Testudines and everything closer to them than to Lepidosauria or Archosauria. (Joyce et al., 2021.)

No vertebrate group is more radically transformed than turtles - a situation that has greatly hampered attempts to ascertain their phylogenetic relationships. We have even complained of lacking the Archaeopteryx of turtles, despite, apparently, having at least one under our noses for a century. Here we start with what's definitely known and work outward.

Major groups

(Joyce et al., 2021.)

Major trends:

Keratinous (above) and bony (below) elements of the shell from Pough et al., 1990.
The turtle shell - Components: A composite structure in several senses:
The turtle shell - Development:

How the components of the carapacial elements form and the precise identity of their homologs has been contentious. Major historic hypotheses include:

Hirasawa et al., 2013, indicate a more subtle process.

in the costals:

Eventually, all suture to form a rigid shell. Thus, the development of the carapace is a little of both:

Trachemys scripta, the red-eared slider - disassembled
In contrast to all other tetrapods:

Ventilating turtle lungs from Pough et al., 1990.
The lungs: Consequences of having a rigid shell that forms in this way:

Pectoral girdles of Captorhinus (left) and Macroclemys - a cryptodire (right)
The girdles: As noted above: this leaves the endochondral elements of the girdles.

Chelydra serpentina, the snapping turtle - quadrate in red
The turtle skull: Characterized by widespread trends:

Diversity of Pantestudines


(Late Jurassic - Quaternary) The crown group of living turtles encompasses two distinct clades: Note: Almost all living turtles retract their heads, but this capacity has evolved independently and happens in different ways. Earlier literature would include creatures from the Late Triassic and Early Jurassic, but recent work including Joyce, 2007 has booted these down onto the stem.

Synapomorphies of Testudines:

Chelodina longicollis the eastern long-necked turtle from Wikimedia.com (left) Terrapene carolina bauri the Florida box turtle of Gloria Lennon (right).


(side-neck - Late Jurassic - Quaternary) (above left)

Side-necked turtles retract their heads flexing their necks at the well developed articulations between cervical centra. Restricted to the southern (gondwanan) continents, they are the dominant turtles of Australia. Their synapomorphies include:

Comparison of stem testudine (left), cryptodiran (center) and pleurodiran trochlear pattern from Joyce, 2007

Pleurodiran superlatives:


(Hidden neck - Late Jurassic - Quaternary) (above right)

The monophyletic group containing all turtles that pull their heads straight into their shells. Synapomorphies include:

Noteworthy plesiomorphy: Otic capsule serves as trochlea for adductor muscles. Among living turtles, this distinguishes cryptodires, but it is also present among stem turtles.

Chisternon a baenid from Wikipedia
Cryptodiran superlatives:

Closest Relatives of Testudines:

The fossil record is full of creatures that are clearly turtles for all intents and purposes but fall outside the Testudines crown. Starting at the crown we move downward.

Meiolania platyceps
Meiolaniidae: (Cretaceous - Quaternary) Terrestrial turtles of the southern continents with: The last species, Meiolania platyceps of Lord Howe Island became extinct only 2000 years ago.

Eileanchelys waldmani: (Middle Jurassic) Briefly noted - the first turtle with recognizable aquatic specializations.

Proganochelys quenstedti
Proganochelys: (Late Triassic) Turtles from farther down the tree are generally similar, with: Of these, the earliest and best documented is Proganochelys (Late Triassic), well known from several specimens. It could not retract its legs, head, or tail into its shell. The neck and tail were studded with free-floating pieces of dermal armor. Nevertheless, it was turtle-like in overall appearance, with a full-blown shell and lacking marginal teeth.

Proganochelys quenstedti
It plesiomorphically displayed:

Carpace fragment of Chinlechelys tenertesta from Studium integrale
Chinlechelys: (Late Traissic) Described by Joyce et al., 2008, the Late Triassic Chinlechelys of Arizona resembles Proganochelys except in that perichondral bone of its ribs and vertebrae are so loosely coossified with their dermal component, that their separate identity is clear. When first described, this seemed to resolve a long-standing enigma. In this early testudinatan, the skeletal elements of the shell seem to form by the coossification of the ribs with preexisting dermal plates, but it was not to be.

Testudinata: (Late Triassic - Quaternary) The last common ancestor of all creatures with complete turtle shells, and all of its descendants. Synapomorphies include:

Stem Testudinata: Now it gets interesting.

Odontochelys semitestacea

Odontochelys semitestacea:

Described by Li et al., 2008, the Late Triassic Odontochelys of China was at the time the most anatomically primitive turtle known. Indeed, it definitely lacks one synapomorphy - the toothless mouth. Odontochelys has typical simple teeth. Stranger yet, although it has a plastron, it lacks a proper carapace.

Distinctive features:

Odontochelys invokes a new big question: Did the plastron evolve before the carapace, or is Odontochelys secondarily derived in having lost its carapace?

Synapomorphies with Testudinata:

PC analysis of combined forelimb and manus measurements from Dudgeon et al., 2021
Odontochelys was found in marine deposits of an embayment that was surrounded on three sides by land. Was it aquatic? That was the initial interpretation of Li et al., 2008 however it:

Eorhynchochelys sinensis from SciNews

Eorhynchochelys sinensis:

Li et al., 2018 Provide a glimpse of a slightly less derived version from the Early Late Triassic of China. Eorhynchochelys has the broadened ribs and flattened puboischiatic plate of turtles, but lacks any kind of plastron, offering a glimpse of the pantestudine condition just prior to that transformation.

But wait! Eorhynchochelys is derived in one respect: Although it retains maxillary teeth, the premaxillae and anterior dentaries seem to support a rhamphotheca!

Eunotosaurus africanus from SciNews

Eunotosaurus africanus:

For a century, we have lamented not having the Archaeopteryx of turtles despite, evidently actually having it. Eunotosaurus africanus: (Middle Permian) Roughly a foot long, with a small head and roly-poly torso supported by expanded dorsal ribs. Known to science since 1892, this animal has alternately been considered close to and far from turtle ancestry.

Eunotosaurus shares with Odontochelys and Testudinata these synapomorphies:

Eunotosaurus is our first glimpse of the broadening of ribs. At this evolutionary stage, they offer little actual protection to the animal, but do:

What selective advantage encouraged their evolution? Lyson et al., 2016 argue that they are an adaptation to fossoriality, providing Eunotosaurus, with a solid base for the origin of powerful limb muscles.

Regardless of how phylogenetic analyses are structured, Eunotosaurus groups with Odontochelys and Testudinata.

Ontogeny and Phylogeny

One story that emerges from this phylogeny involves the position of the pectoral girdle with respect to the ribs. Ontogenetically, the scapula first forms in the normal position, but is able to slip beneath the carapace because the anterior ribs become angled posteriorly. Phylogenetically we see the same sequence:

The Position of Pantestudines - May, 2015

Follow the bouncing turtles: When we try to say anything about the position of turtles in the tree of amniote evolution, things quickly get weird. Of all recent phylogenetic enigmas, turtles have been the most intractable.

Chronology of phylogenetic hypotheses:

Data type and results

Molecular analyses: For twenty years, relationships of Testudines to other extant groups have been addressed by molecular systematics. At various points they have been recovered as sister taxon to: By far the strongest pattern has been as sister to Archosauria, causing many authorities to accept the relationship. There are zero morphological synapomorphies uniting turtles and archosaurs.

The last decade: Other lines of evidence have been brought to bear on the issue of turtle relationships and the homologies of their skeletal elements.

2015 - Summer of Revelation:

When we taught GEOL431 in 2015, the accumulating morphological and developmental data seem to support the parareptilian hypothesis of turtle origins. Then came an interesting summer:

Pappochelys rosinae from Carnivora
Pappochelys rosinae (Middle Triassic of Germany) was described by Schoch and Sues, 2015. This small (~30 cm overall length) animal is intermediate between Eunotosaurus and Odontochelys both in time and morphology: They are clearly closely related.

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.
Not actually. The skull roof of Eunotosaurus is covered with dermal bone, however it has an odd feature: the supratemporal projects far anteriorly. By digitally removing it form high-resolution CT scans, Bever et al., 2015 revealed that it covered a proper supratemporal fenestra. Moreover, they showed ontogenetic variation in the development of the anterior extension of the supratemporal bone. Juveniles, it developed, had proper supratemporal fenestrae.

Why would Eunotosaurus do this?

And what does this tell us about the importance of fenestration patterns as "key characters" in taxonomy? :-(

Eunotosaurus africanus skull reconstruction from Bever et al., 2015.

Candelaria barbouri, an owenettid procolophonoid from Cisneros et al., 2004.


But note, in some ways Eunotosaurus really isn't what we expect of saurian or nearly saurian turtle precursor: Indeed, Lichtig and Lucas, 2021, in their redescription of Chinlechelys, reaffirm that turtles belong in Parareptilia, and denounce Eunotosaurus and Pappochelys as red-herrings that are not close turtle relatives. We still await consensus.

Pantestudines, as of Summer, 2015. The end?

So what are they?

Do we just shrug our shoulders and admit that turtles belong in Archosauria? Not yet! Two issues to consider: We hope for salvation through future revelations. Until then, Schoch and Sues, 2019 provide an excellent review.


Additional reading:

Eunotosaurus skull reconstruction from Bever et al., 2015.