"God's noblest creation"
And now, a problem....
Testudo, Malaclemys terrapin, the diamond-back terrapin
Stupendemys geographicus, the largest turtle ever
Pantestudines(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.
- Testudines: The crown group of living turtles. Includes:
- Cryptodira: the mid-line head-retracting turtles
- Pleurodira: the side-necked turtles
- Testudinata: The apomorphy-based (!) group including living turtles and all members of their fossil stem with a complete turtle shell, including carapace with interlocking costals, neurals, peripherals, and a nuchal; and plastron ((Joyce et al., 2021.))
- Assorted stem-testudinatans and stem-pantestudines.
Keratinous (above) and bony (below) elements of the shell from Pough et al., 1990.
- A dorsal carapace is integrated with a ventral plastron between the fore and hindlimbs. These sections form by distinct developmental processes and did not evolve simultaneously.
- Both carapace and plastron have:
- a bony endochondral skeleton
- a covering of broad keratinous scales.
Keratinous (left) and bony (right) elements of the shell in snapping turtle, Chelydra serpentina
Plastron elements from LafeberVet
- While the bones of the plastron are modified variants of those in other tetrapods:
- Epiplastron = clavicle
- Entoplastron = interclavicle
- Remainder = gastralia
Ventral view of carapace of Apolone spinifera (on its back)
- Neurals incorporate dorsal vertebrae
- Costals incorporate ribs
- Marginals, suprapygal, and pygal have no obvious homologs
- The nuchal's homologies are contentious (see below).
How the components of the carapacial elements form and the precise identity of their homologs has been contentious. Major historic hypotheses include:
- The osteoderm hypothesis: maintains that the ribs and vertebrae fused developmentally with preexisting dermal scutes.
- The de novo hypothesis: holds that all of the shell elements are direct outgrowths of ribs and vertebrae.
Trachemys scripta, the red-eared slider - disassembled
- The ribs initially form in the somitic sclerotome but do not extend ventrally into the lateral plate mesoderm forming the body wall. Instead, they invade the dermis of the dorsal trunk.
- Rib formation is partially induced by the carapacial ridge that extends around the trunk. This feature functions like the apical ectodermal ridge of the limb buds, attracting the growing ribs and deflecting them from their normal developmental pathway. (Hirasawa et al., 2014)
- The elements of the plastron, in contrast seem to form from a secondary proliferation of neural crest, according to Clark et al., 2001.
Ventilating turtle lungs from Pough et al., 1990.
- The girdles are enclosed inside the shell. (Not strictly inside the rib cage when one disregards shell components that aren't strictly homologous with ribs.)
- There is no room for intercostal muscles normally used to expand and contract the rib cage in breathing.
- Breathing is facilitated by the action of muscles on the:
- posterior limiting menbrane posteriorly
- and on the pectoral girdle anteriorly.
Pectoral girdles of Captorhinus (left) and Macroclemys - a cryptodire (right)
- The turtle clavicle and interclavicle are incorporated into the plastron
- The cleithra are a puzzle:
- The pectoral girdle is triradiate with:
- a long, slender scapular shaft,
- a very long acromion process of the scapula,
- and a broad anterior coracoid.
- the pelvis connects to the carapace through two pairs of sacral ribs, and abuts the plaston ventrally. (Among pleurodires, it fuses to the shell top and bottom.)
Chelydra serpentina, the snapping turtle - quadrate in red
- Marginal and palatal teeth lost
- Jaws lined by a rhamphotheca (keratinous beak) as in birds and dicynodonts
- The adductor muscles of the jaw pass over the otic capsule, which acts like a pulley.
- The basipterygoid articulation is fused. (Compare with Petrolacosaurus.)
- The skull is anapsid, yet there is often (but not always) significant emargination of the temporal skull roof by embayments from the occipital region and the lower cheek margin. (An extreme case.)
Diversity of Pantestudines
Testudines:(Late Jurassic - Quaternary) The crown group of living turtles encompasses two distinct clades:
- Cryptodira: the mid-line head-retracting turtles (familiar to North Americans)
- Pleurodira: the side-necked turtles (limited to the southern continents)
Synapomorphies of Testudines:
- Complete loss of palatal teeth
- Reduction of cervical ribs
- Reduction in tenth (posterior) dorsal rib
- Increase in number of pedal and manual phalanges
Chelodina longicollis the eastern long-necked turtle from Wikimedia.com (left) Terrapene carolina bauri the Florida box turtle of Gloria Lennon (right).
Pleurodira:(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
- Presence of a trochlear process of the pterygoid to guide the adductor muscles (right).
- Loss of the epipterygoid
- Presence of an anterior extension to the braincase wall
- Median contact of the posterior costals to form a suprapygal.
- Procoelous caudal vertebrae
- Pelvis solidly fused to shell
- Stupendemys (Neogene of Venezuela) Fresh water aquatic. The largest turtle ever.
- Chelus fimbriata, the mata mata of South America. A cryptic turtle that has lost its beak and depends entirely on suction feeding.
- Chelodina longicollis, the Australian eastern long-necked turtle.
Cryptodira:(Hidden neck - Late Jurassic - Quaternary) (above right)
The monophyletic group containing all turtles that pull their heads straight into their shells. Synapomorphies include:
- Presence of an anterior extension to the braincase wall (convergent with Pleurodira!)
- Pterygoid - basisphenoid contact conceals basipterygoid articulation.
- Retraction of neck along sagittal plane facilitated by accessory articulations of the neural arches
Chisternon a baenid from Wikipedia
- Paracryptodira: (Late Jurassic - Paleogene) Near the cryptodire/pleurodire split, including the common Baenidae (right). Abundant fresh water turtles of the Cretaceous and Paleogene.
- Chelonioidea: (Cretaceous - Quaternary) Sea turtles, the only turtles successfully to invade the open oceans, including the largest living turtle (the leatherback) and Cretaceous superlatives like Protostega.
- Trionychia: (Cretaceous - Quaternary) Including pig-nosed turtles and softshelled turtles - fresh water turtles with reduced carapaces and limbs modified for rapid swimming.
- Testudinoidea: (Paleogene - Quaternary) Including tortoises and pond turtles.
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.
- robust cranial horns and bosses
- long armored tails (independently derived)
Eileanchelys waldmani: (Middle Jurassic) Briefly noted - the first turtle with recognizable aquatic specializations.
- Terrestrial adaptations (Illuminated by Joyce and Gauthier, 2004)
- Armored necks and tails
- Palatal teeth
- The absence of a trochlear system of the jaws
- A mobile basipterygoid articulation
- A clavicle (or is that "epiplastron?") with a dorsal process that reached the carapace.
- A relatively short acromion process.
Carpace fragment of Chinlechelys tenertesta from Studium integrale
Testudinata: (Late Triassic - Quaternary) The last common ancestor of all creatures with complete turtle shells, and all of its descendants. Synapomorphies include:
- Ten dorsal vertebrate present
- Costal elements sutured together
- Nuchal, pygal, and costal elements present
Now it gets interesting.
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.
- Its depositional environment and limb shape indicates that it was aquatic.
- It's ribs are expanded into paddle-shapes, but
- there are no endochondral dermal scutes associated.
- Some living highly aquatic turtles have reduced their carapaces significantly.
- However the plastron forms from a secondary proliferation of neural crest, a distinct developmental pathway from the carapace.
Synapomorphies with Testudinata:
- Paired gastralia transformed into plastron
- Addition of two cervical vertebrae
- incipient development of dorsal vertebrae into neural plates
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:
- is discordant with other animals in this part of the tree
- is not strongly supported anatomically. Joyce, 2015 maintains that the morphology of the phalanges indicates terrestriality in that the articulation of the first phalanx in each digit highly flexible.
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:
- Reduced number of dorsal vertebrae
- Dorsal vertebrae elongate compared to cervicals and sacrals
- Dorsal ribs perichondrally expanded
- Judging from histology, intercostal muscles did not span the gaps between dorsal ribs.
- Trunk is wide
- Paired gastralia (however these are normal-looking)
Eunotosaurus is our first glimpse of the broadening of ribs. At this evolutionary stage, they offer little actual protection to the animal, but do:
- Reduce its stride length by making the trunk inflexible
- Reduce the ability to ventilate the lungs
Regardless of how phylogenetic analyses are structured, Eunotosaurus groups with Odontochelys and Testudinata.
Ontogeny and PhylogenyOne 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:
- In Eunotosaurus the scapular blade is oriented dorsally anterior to the rib cage.
- In Odontochelys the dorsal process of the scapula is short and well anterior to the ribs because the distal ends of the ribs are squeezed together anteroposteriorly
- In Proganochelys the ribs (as costals) have resumed their normal orientation but the scapula is now ventral to them.
The Position of Pantestudines - May, 2015Follow 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:
- Gaffney and Meylan, 1988, deemed them to be related to captorhinids, basal eureptiles.
- Reisz and Laurin, 1991 indicated a possible close relationship between turtles and procolophonoids.
- Lee, 1993 proposed Pareiasaurs as a sister taxon. (In fact, according to later work by Lee, Pareiasaurs may be paraphylteic with respect to turtles, i.e. turtles may be a kind of pareiasaur.) Lee's argument assumed that the dermal component of the turtle shell derived from preexisting osteoderms.
- Rieppel and deBraga, 1996 performed a morphological cladistic analysis that placed turtles inside Lepidoauria, as members of Euryapsida, alongside sauropterygians. An interesting result for what it says about euryapsids! Traditionally turtle armor is seen as fundamentally different from that of armored placodonts but this result prompted open reconsideration.
- Lyson et al., 2010 re-ran the Rieppel and deBraga 1996 matrix adding Eunotosaurus and Proganochelys. The effect was that Eunotosaurus grouped as the sister taxon of Testudinata, inside Parareptilia.
Data type and resultsMolecular 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:
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.
- 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 Sauria. (Of course only living taxa could be considered in this way. Maybe outside of Diapsida.)
- Werneburg et. al, 2013 examined the development of the turtle neck, identifying embryonic intercentra and ribs that become coossified into cervical vertebrae. Among saurians, intercentra are greatly reduced, so their presence among turtles appears to argue for a non-saurian origin.
- The central 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 bone (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, again, argues against their being members of Sauria.
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
- 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? :-(
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:
Pappochelys is informally reported (Sues, 2015 pers. comm.) to have:
- a facet for the cleithrum on its scapula. Moreover, evidence for cleithra is reported for Kayentachelys (Joyce et al., 2006) and Eileanchelys (Anquetin et al., 2008) as well.
- no descending flanges of the parietal
That indicates that although they may be diapsids, they are outside of Sauria.
- In a stunning reversal, Lichtig and Lucas, 2021, in their redescription of Chinlechelys, reaffirm that turtles belong in Parareptilia, and that Eunotosaurus and Pappochelys are red-herrings that are not close turtle relatives. Your instructors are skeptical, but we await clarification.
- Finally, no morphological data can really refute the molecular data that suggest that turtles are archosaurs. Indeed, it is difficult to compare these data directly.
- Anquetin, J., Barrett, P.M., Jones, M.E.H., Moore-Fay, S., and Evans, S. 2008. A new stem turtle from the Middle Jurassic of Scotland: new insights into the evolution and palaeoecology of basal turtles. Proceedings of the Royal Society B, 276:879-886. https://doi.org/10.1098/rspb.2008.1429
- G. S. Bever, Tyler R. Lyson, Daniel J. Field, and Bhart-Anjan S. Bhullar, 2015. Evolutionary origin of the turtle skull. Nature 525: 239-242.
- K. Clark, G. Bender, B.P. Murray, K. Panfilio, R. Davis, K. Mumen, R.S. Tuan, S. F. Gilbert, 2001. Evidence of the neural crest origin of turtle plastron bones. Genesis 31(3): 111-117.
- Eugene Gaffney, 1990. The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the American Museum of Natural History. 194. 261 pp.
- Eugene Gaffney and Peter Meylan, 1988. A phylogeny of turtles. pp. 157-219 in M.J. Benton (ed.) The Phylogeny and Classification of the Tetrapods, Vol.1, Clarendon Press, Oxford, 1988.
- Tatsuya Hirasawa, H Nagashima, Shigeru Kuratani, 2013. The endoskeletal origin of the turtle carapace. Nature Communications. 4: 2107.
- Tatsuya Hirasawa, Juan Pascual-Anaya, Naoki Kamezaki, Mari Taniguchi, Kanako Mine, and Shigeru Kuratani, 2014. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. Journal of Experimental Zoology (Mol. Dev. Evol.) 324B: 194-207.
- Walter Joyce and Jacques Gauthier, 2004. Palaeoecology of triassic stem turtles sheds new light on turtle origins. Proceedings in Biological Science 7:271(1534):1-5.
- Joyce, W.G., Jenkins, F.A., and Rowe, T.R. 2006. The presence of cleithra in the basal turtle Kayentachelys aprix. Fossil Turtle Research, 1:93-103.
- Walter Joyce, 2007. Phylogenetic relationships of Mesozoic turtles. Bulletin of the Paebody Museum of Natural History 48(1): 3-102.
- Walter Joyce, Spencer Lucas, Torsten Scheyer, Andrew Heckert, and Adrian Hunt, 2009. A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell. Proceedings of the Royal Society B.276: 507-513.
- Walter Joyce, 2015. The origin of turtles: A paleontological perspective. Journal of Experimental Zoology (Mol. Dev. Evol.) 324B: 181-193.
- Walter G. Joyce, Jeremy Anquetin, Edwin-Alberto Cadena, Julien Claude, Igor G. Danilov, Serjoscha W. Evers, Gabriel S. Ferreira, Andrew D. Gentry, Georgios L. Georgalis, Tyler R. Lyson, Adán Pérez-García, Márton Rabi, Juliana Sterli, Natasha S. Vitek and James F. Parham, 2021. A nomenclature for fossil and living turtles using phylogenetically defined clade names. Swiss Journal of Palaeontology, 140: 5.
- Michael Lee, 1993. The origin of the turtle body plan: bridging a famous morphological gap. Science 261: 1716-1720.
- Chun Li, Nicholas C. Fraser, Olivier Rieppel, and Xiao-Chun Wu, 2018. A Triassic stem turtle with an edentulous beak. Nature 560, 476–479.
- Chun Li, Xiao-Chun Wu, Olivier Rieppel, Li-Ting Wang, and Li-Jun Zhao, 2009. an ancestral turtle from the Late Triassic of southwestern China. Nature 456/27.
- Asher J. Lichtig and Spencer G. Lucas, 2021. Chinlechelys from the Upper Triassic of New Mexico, USA, and the origin of turtles. Palaeontologica Electronica: 24.1.a13.
- Tyler Lyson, Gabe Bever, Bhart-Anjan Bhuller, Walter Joyce, and Jacques Gauthier, 2010. Transitional fossils and the origin of turtles. Biology Letters 6, 830-833.
- Tyler Lyson, Gabe Bever, Torsten Scheyer, Allison Hsiang, and Jacques Gauthier, 2013. Evolutionary Origin of the Turtle Shell. Current Biology 23, 1113-1119.
- Tyler Lyson, Bruce S. Rubidge, Torsten M. Scheyer, Kevin de Queiroz, Emma R. Schachner, Roger M.H. Smith, Jennifer Botha-Brink, G.S. Bever, 2016. Fossorial Origin of the Turtle Shell. Current Biology 26, 1887-1894.
- Sean Modesto, 2000. Eunotosaurus africanus and the Gondwanan ancestry of anapsid reptiles. Palaeontologia Africana 36: 15–20.
- Robert Reisz and Michel Laurin, 1991. Owenetta and the origin of turtles. Nature 349:324-326.
- Olivier Rieppel and Michael DeBraga, 1996. Turtles as diapsid reptiles. Nature 384: 453-455.
- Rainer Schoch and Hans-Dieter Sues, 2015. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523: 584-587.
- Ingmar Werneburg, Wolfgang Maier, Walter Joyce, 2013. Embryonic remnants of intercentra and cervical ribs in turtles. Biology Open 000: 1-5.
- Ingmar Werneburg and Marcelo Sanchez-Villagra, 2009. Timing of organogenesis support basal position of turtles in the amniote tree of life. Evolutionary Biology 9:82.
- G. S. Bever, Tyler R. Lyson, Daniel J. Field, and Bhart-Anjan S. Bhullar, 2015. Evolutionary origin of the turtle skull. Nature 525: 239-242.