Turtle body plans 2020: still not diapsids

Lyson and Bever 2020 once again propose
a diapsid origin for turtles that is not supported by the large reptile tree (LRT, 1719+ taxa, subset Fig. 1) where hardshell and soft-shell turtles arise in parallel from small horned pareiasaurus without temporal fenestrae — and all competing candidates for turtle ancestry are tested.

From the Lyson and Bever abstract:
“The origin of turtles and their uniquely shelled body plan is one of the longest standing problems in vertebrate biology.”

In the LRT this problem has been resolved for several years. Click here for an online paper on the dual origin of turtles from pareiasaurs. Click here for the dual origin of turtles to scale blogpost. Click here for the latest LRT cladogram.

“The unfulfilled need for a hypothesis that both explains the derived nature of turtle anatomy and resolves their unclear phylogenetic position among reptiles largely reflects the absence of a transitional fossil record.”

Not so. In the LRT several overlooked taxa well document a good transitional fossil record. Lyson and Bever omit, ignore and overlook these taxa in favor of several unrelated turtle mimics.

“Recent discoveries have dramatically improved this situation, providing an integrated, time-calibrated model of the morphological, developmental, and ecological transformations responsible for the modern turtle body plan. This evolutionary trajectory was initiated in the Permian (>260 million years ago) when a turtle ancestor with a diapsid skull evolved a novel mechanism for lung ventilation. This key innovation permitted the torso to become apomorphically stiff, most likely as an adaption for digging and a fossorial ecology. The construction of the modern turtle body plan then proceeded over the next 100 million years following a largely stepwise model of osteological innovation.”

Not so. Overlooked taxa known for decades (Elginia (Fig. 2), Sclerosaurus) have been traditionally excluded from turtle origin studies. Some recent discoveries (Eorhynochelys, Pappochelys) nest elsewhere, apart from turtles, as turtle mimics. The LRT tests all known candidates. Lyson and Bever do not. They are still excluding pertinent taxa. Adding more taxa shows that turtles and their ancestors have never been diapsids.

Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

The most primitive hardshell turtles 
are not the oldest known hardshell turtles. Horned turtle skulls are widely and traditionally considered derived, not primitive. Elginia and Meiolania (Fig. 2) have never been tested together in analysis, and not by Lyson and Bever, despite their obvious similarities and homologies.

Turtle respiration was a big issue for Lyson and Bever.
Earlier we looked at pre-softshell turtle respiration in Sclerosaurus here.

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Turtle mimics are out there.
Evidently only a wide gamut phylogenetic analysis, like the LRT, can lump and separate turtle ancestors from turtle mimics without bias and without traditional influences. Lyson and Bever mistakenly accepted several turtle mimics as turtle ancestors, then built a diapsid story around their cherry-picked taxa. Referees and editors also accepted this invalid scenario.

Add taxa
to find and separate real turtle ancestors from turtle mimics.


References
Lyson TR and Bever GS 2020. Origin and Evolution of the Turtle Body Plan Annual Review of Ecology, Evolution, and Systematics 51:- (Volume publication date November 2020) Review in Advance first posted online on July 31, 2020. (Changes may still occur before final publication.) https://doi.org/10.1146/annurev-ecolsys-110218-024746

researchgate.net/_The_dual_origin_of_turtles_from_pareiasaurs

Sclerosaurus and the evolution of turtle respiration

Lyson et al. 2014 brought us their view
on the origin of ventilation (= respiration) in turtles using fossils and extant taxa. Similarly, and in the same year, Hirasawa et al. 2014 did the same from a different perspective: turtle embryos.

Unfortunately
neither put their finger on the correct phylogenetic origins of turtles (Fig. 1) due to taxon exclusion. You can’t get a valid phylogenetic solution without a valid phylogeny.

Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

Figure 2. Subset of the LRT focusing on the dual turtle clades (pink) and their ancestors.

Both sets of authors
overlooked/omitted the ancestor taxa of turtles recovered by the large reptile tree (LRT, 1694+ taxa; subset Fig. 1), which tested all current candidates for turtle ancestry. That means both sets of authors stepped into the morass that is convergence.

Figure 8. Sclerosaurus insitu. This turtle ancestor still bas a flexible spine, but the pectoral girdle has migrated anterior to the dorsal ribs. A hypoischiuum is present.

Figure 2. Sclerosaurus insitu. This turtle ancestor still bas a flexible spine, but the pectoral girdle has migrated anterior to the dorsal ribs. A hypoischiuum is present.

Here,
the LRT (subset Fig. 1) minimizes taxon exclusion due to its wide gamut of included taxa. Here turtles had dual origins from small horned pareiasaurs. Basal to hard-shell turtles, Elginia documents the genesis of cranial traits. Post-crania is poorly known. Basal to soft-shell turtles, Sclerosaurus (Figs. 2–4) documents the genesis of soft-shell turtle traits. These remain (at present) the best clues we have to the genesis of stem hard-shell turtle post-cranial traits. Those are lacking until we go back to the large pareisaur Bunostegos.

Figure 1. Softshell turtle ancestor, Sclerosaurus animated walking in dorsal view. Dorsal armor initially does nothing to prevents lateral undulation here, as shown by the in situ fossil.

Figure 1. Softshell turtle ancestor, Sclerosaurus animated walking in dorsal view. Dorsal armor initially does nothing to prevents lateral undulation here, as shown by the in situ fossil.

Key to the present discussion,
Sclerosaurus had a wide set of dorsal ribs that were not immobilized by the sprinkling of armor over the dorsal vertebrae. The specimen (Fig. 2) is preserved bending far to the left. So it undulated when it walked (Fig. 3). Sclerosaurus lacked a plastron and/or gastralia.

Figure 4. Sclerosaurus walking with an imagined ventral cross-brace, a plastron. Now this more closely resembles turtle locomotion.

Figure 4. Sclerosaurus walking with an imagined ventral cross-brace, like a turtle plastron. Now Scleromochlus locomotion more closely resembles turtle locomotion. Compare to figure 1.

Immobilzation of the thorax in soft shell turtles
occurs with the genesis of the plastron in Odontochelys (Fig. 5). If we give Sclerosaurus a hypothetical ventral cross brace to stiffen its thorax in the above animated graphic (Fig. 4), it suddenly walks like a turtle (Fig. 4). At first that permits breathing while walking by overcoming Carrier’s constraint. Extant turtles have such a low metabolism that breathing is the last thing they think to do. Sea turtles hold their breath for long periods underwater.

Immobilization of the thorax in Odontochelys
prevented costal ventilation (expanding the ribcage). This is reflected in turtle embryos, which lose intercostal muscles as they develop a rigid shell, according to Hirasawa et al. 2014. Three sets of internal thoracic (hypaxial) muscles take over respiration, expanding to press on the lungs between them or relaxing to initiate inspiration, according to Lyson et al. 2014.

Figure 3. Sister taxa according to Bever et al. Eunotosaurus purportedly nests between Ascerosodontosaurus and the turtles. The large reptile tree, on the other hand, finds that only the turtles are related to each other.

Figure 5. Sister taxa according to Bever et al. Eunotosaurus purportedly nests between Ascerosodontosaurus and the turtles. The large reptile tree, on the other hand, finds that only the turtles are related to each other.

Lyson et al. 2014 
suggested, “the ventilation mechanism of turtles evolved through a division of labour between the ribs and muscles of the trunk in which the abdominal muscles took on the primary ventilatory function, whereas the broadened ribs became the primary means of stabilizing the trunk.” Unfortuantely their ‘early member of the turtle stem lineage’ was the unrelated turtle mimic, Eunotosaurus (Figs. 5, 6). We discussed taxon exclusion errors several times earlier here, here and here.

Figure 3. Subset of the LRT with Martensius added to the base of the Caseasauria + another clade of similar lepidosaurs, all derived from Milleretta.

Figure 6. Subset of the LRT with Martensius added to the base of the Caseasauria + another clade of similar lepidosaurs, all derived from Milleretta. Note the placement of Eunotosaurus with sisters, none of which is close to turtles in the LRT.

Lyson et al. hypothesized,
“an easing of structural constraints through division of function (divergent specialization) between the dorsal ribs and the musculature of the body wall facilitated the evolution of both the novel turtle lung ventilation mechanism and the turtle shell.”
This is likely correct, but they used the wrong outgroup taxon, a turtle mimic, rather than a valid stem turtle. Lyson et al. thought the initial thoracic stiffening occurred in the carpace, as it does in Eunotosaurus, which lacks a plastron or more than 5 pairs of slender gastralia not in the radiating pattern of a plastron. Some Eunotosaurus specimens have overlapping ribs. Turtles don’t do this. Mutual side-by-side suturing is the turtle rib pattern and that’s just the beginning of a long list of non-turtle traits found n Eunotosaurus, which nests with Acleistorhinus and other near caseids in the LRT (Fig. 6), all with lateral temporal fenestrae, making them all synapsid mimics.

As you’ll note above,
Sclerosaurus does not have expanded ribs. They begin to expand with Odontochelys (Fig. 5). By contrast, the turtle-mimic, Eunotosaurus, has much more expanded dorsal ribs than those in Odontochelys. That’s the reverse of the order one would expect. The LRT indicates that Lyson et al. should have expanded their taxon list. Sins of omission are also considered sins in paleontology.

Lyson et al. fell prey to a classic error in paleontology
when they ‘Pulled a Larry Martin,‘ listing traits the turtle mimic, Eunotosaurus, shares with turtles. That’s why a good taxonomist saves listing traits until AFTER a comprehensive phylogenetic analysis determines what is related to what and what converges with what.

Hirasawa et al. 2014
attempted to provide ‘answers to the question of the evolutionary origin of the carapace… Along the line of this folding develops a ridge called the carapacial ridge (CR), a turtle‐specific embryonic structure.’ More important to the present discussion is the genesis of the plastron.

A little backstory on Sclerosaurus
Sclerosaurus armatus (Meyer 1859) Middle Triassic ~50 cm in length, was originally considered a procolophonid, then a pareiasaurid, then back and forth again and again, with a complete account in Sues and Reisz (2008) who considered it a procolophonid.

Here, based on data from Sues and Reisz (2008), Sclerosaurus nests between pareiasaurs and basal softshell turtles like ArganacerasOdontochelys and Trionyx. Their analysis also suffered from taxon exclusion. Sclerosaurus is also a sister to another small horned pareiasaur, Elginia and thus is only slightly more distantly related to Meiolania, the hard-shelled horned basalmost turtle in the LRT.

Overall smaller than other pareiasaurs, Sclerosaurus had a wide, flat body, like the horned lizard, Phrynosoma. The backbone remained quite flexible, as shown by the in situ fossil. Only a sparse sprinking of dermal bones lined the dorsal vertebrae. Note the hypoischium posterior to the ischium and the position of the pectoral girdle anterior to the dorsal ribs, as in Odontochelys.


References
Hirasawa T, Pascual‐Anaya J, Kamezaki N, Taniguchi M, Mine K and Kuratani S. 2015. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. J. Exp. Zool. (Mol. Dev. Evol.) 324B:194–207.
Lyson TR et al. (7 co-authors) 2014. Origin of the unique ventilatory apparatus of turtles. Nature Communications 5:5211.
Meyer H von 1859. Sclerosaurus armatus aus dem bunten Sandestein von Rheinfelsen. Palaeontographica 7:35-40.
Sues H-D and Reisz RR 2008. Anatomy and Phylogenetic Relationships of Sclerosaurus armatus (Amniota: Parareptilia) from the Buntsandstein (Triassic) of Europe. Journal of Vertebrate Paleontology 28(4):1031-1042. doi: 10.1671/0272-4634-28.4.1031 online

wiki/Sclerosaurus

Origin of turtle body plan: Schoch and Sues 2019

Schoch and Sues 2019 once again bring us
their invalidated scenario for the origin of turtles (= Odontochelys and Proganochelys) from traditional ancestors Pappochelys, Eunotosaurus and Eorhynochelys (Fig. 1, bottom) that nest elsewhere in the large reptile tree (LRT, 1612+ taxa; subset Fig. 5), which tests these taxa AND pertinent taxa that Schoch and Sues ignore.

Figure 1. Competing turtle origin hypotheses. Bottom: from Schoch and Sues 2019. Top: From the LRT, which tests all taxa from Schoch and Sues, then adds over 1000 more.

Figure 1. Competing turtle origin hypotheses. Bottom: from Schoch and Sues 2019. Top: From the LRT, which tests all taxa from Schoch and Sues, then adds over 1000 more. On the top left are soft-shell turtles and in. On the top right are hardshell turtles and kin. Note the longer tails n club-tailed taxa ignored by Schoch and Sues. Note the use of freehand drawings, which allows bias to creep in and draws us further from the raw data.

Unfortunately,
Schoch and Sues 2019 do not examine and describe the actual ancestors of turtles recovered by the LRT, Stephanospondylus, Bunostegos, Elginia and Sclerosaurus. And because of this they do they do not realize that turtles had a dual ancestry within small, horned pareiasaurs (Fig. 1). Instead, Schoch and Sues cherry-picked their taxa and made up a ‘just-so’ story.

Schoch and Sues are not aware of ‘The Big Picture’
that the first dichotomy splitting all reptiles is the Lepidosauromorpha / Archosauromorpha split. Instead they rely on traditional tree topologies (many of them invalid genomic studies) that do not go back to the origin of reptiles and do not include pertinent taxa. Uncritically they rely on the flawed work of others.

Schoch and Sues do not realize
how rampant convergence is within the Tetrapoda, including the Reptilia. They do not realize that only a wide gamut phylogenetic analysis that recovers a well-resolved tree can correctly nest taxa. Instead they ‘pull a Larry Martin’ and hope the traits and taxa they pick are correct. They are not correct based on testing a wider gamut of taxa in the LRT.

The LRT tells a better ‘just-so’ story
because it does not omit key taxa. And it nests the ancestors hanbd-picked by Schoch and Sues far from turtles on the LRT.

When Pappochelys was added to the LRT,
(Fig. 2) it nested at the base of the Placodontia along with Palatodonta, between Diandongosaurus and Palacrodon and the rest of the placodonts, some of which also had broad ribs and gastralia, all far from turtles. Some placodonts even became turtle mimics.

Figure 6. Pappochelys compared to placodont sister taxa and compared to the Schock and Sues reconstruction, which appears to have several scale bar errors and underestimated the number of dorsal vertebrae. Click to enlarge. So few ribs and vertebrae are known for Pappochelys that their order, size and number could vary from that shown here. Note the ribs of Paraplacodus are also expanded. The number of dorsal vertebrae is unknown and probably more than nine based on sister taxa.

Figure 2. Pappochelys compared to placodont sister taxa and compared to the Schock and Sues reconstruction, which appears to have several scale bar errors and underestimated the number of dorsal vertebrae. Click to enlarge. So few ribs and vertebrae are known for Pappochelys that their order, size and number could vary from that shown here. Note the ribs of Paraplacodus are also expanded. The number of dorsal vertebrae is unknown and probably more than nine based on sister taxa.

Shoch and Sues 2019
discuss several hypotheses from a hundred years ago or more. They report, “Goodrich (1916) already considered it likely that the absence of temporal openings in turtles represented a secondary condition. His hypothesis has received strong support from the discovery of the Middle Triassic stem-turtle Pappochelys, which has two clearly defined temporal openingson either side of the cranium (Schoch & Sues 2015, 2018).” Seems to fit their scenario, so why not? Testing other candidates (Fig. 1) was apparently never considered.

Not sure why Schoch and Sues keep pursuing this myth.
This is John Ostrom’s lament. Paleontology has always moved at a snail’s pace. Why? Perhaps because workers avoid testing previously published papers and cladograms. It’s not that much work. All they have to do is add taxa, like I do, and the software does the rest.

When the turtle mimics,
Eunotosaurus (Fig. 6) and Eorhinchochelys (Fig. 7), were added to the LRT, they nested together, but with Acleistorhinus and Microleter, taxa also omitted from Schoch and Sues 2019.

Figure 2. Shoch and Sues compared Pappochelys to Odontochelys and Proganochelys, but deleted the more primitive Eunotosaurus. And it's easy to see why. Eunotosaurus has wider ribs than its two purported successors. That and the LRT tell you its not a turtle, but a turtle mimic. Note the inaccuracy Schoch and Sues applied to their Odontochelys. The version from ReptileEvolution.com appears in frame 2 of this GIF animation.

Figure 3. Shoch and Sues compared Pappochelys to Odontochelys and Proganochelys, but deleted the more primitive Eunotosaurus. And it’s easy to see why. Eunotosaurus has wider ribs than its two purported successors. That and the LRT tell you its not a turtle, but a turtle mimic. Note the inaccuracy Schoch and Sues applied to their Odontochelys. The version from ReptileEvolution.com appears in frame 2 of this GIF animation.

Figure 2. Eorhynchochelys in situ alongside manus, pes, pectoral and pelvic girdle, plus Eunotosaurus to scale. By convergence Eorhynchochelys resembles Cotylorhychus.

Figure 4. Eorhynchochelys in situ alongside manus, pes, pectoral and pelvic girdle, plus Eunotosaurus to scale. By convergence Eorhynchochelys resembles Cotylorhychus.

Details:
Schoch and Sues 2019 report, “Specifically, we consider four interconnected issues:

  1. what are the closest relatives of turtles among extant reptiles: lepidosaurs (squamates and rhynchocephalians) or archosaurs (crocodylians and birds);
  2. what are the closest relatives of turtles among extinct amniotes;
  3. how does the bony shell develop in extant turtles; and
  4. how did the bony shell evolve in stem-turtles.

Unfortunately
Schoch and Sues do little first hand testing, they rely on genomics and, worst of all, omit taxa that are key to understanding turtle origins (Fig. 8).

Figure 5. Subset of the LRT focusing on turtle origins and unrelated eunotosaurs.

Figure 5. Subset of the LRT focusing on turtle origins and unrelated eunotosaurs. Pappochelys nests on a completely different branch of the Reptilia, the Archosauromorpha, close to the base of the Enaliosauria.

Ironic (= by convergence)
that I the updated turtle video came out a few days ago. Here it is again.

I still find it wondrous
that soft-shell turtles and hard-shell turtles evolved so many trait in parallel with roots among the small horned pareiasaurs. It’s all so obvious once you get them together.


References
Schoch RR and Sues H-D 2015. A new stem-turtle from the Middle Triassic of Germany and the evolution of the turtle body plan. Nature, 523: 584–587.
Schoch RR and Sues H-D 2018. Osteology of the stem-turtle Pappochelys rosin and the early evolution of the turtle skeleton. Journal of Systematic Palaeontology, 16: 927–965.
Schoch RR and Sues H-D 2019. The origin of the turtle body plan: evidence from fossils and embryos. Palaeontology 2019:1–19.

Read the ResearchGate.net paper on the dual origin of turtles here.

Updated Origin of Turtles video on YouTube

This update
to the original Origin of Turtles YouTube video documents the dual origin of turtles (PDF avaialble on Resarchgate.net) that was not covered in the earlier video, now deleted. This hypothesis was recovered from the large reptile tree (LRT) which now tests 1612 taxa (subset Fig. 2). Other that the turtles themselves, the rest of the included taxa (from birds to fish) are all competing to be the closest outgroup(s) to the turtles. All other candidate taxa, like Eunotosaurus and Pappochelys, are tested in the LRT and featured in the video.

This is a seven-minute video
unfortunately with another eleven minutes of black soundless screen tacked on at the end. Not sure how that happened, but there you are. I would have attempted a repair, but YouTube does not permit identical or near identical videos to be uploaded.

If you want to learn more
about the dual origin of turtles by reading an academic paper on the subject, click this link to ResearchGate.net.

Figure 3. Subset of the large reptile tree (LRT, 1199 taxa) with the addition of three basal turtles

Figure 2. Subset of the large reptile tree (LRT, 1612 taxa) focusing on basal turtles

Abstract from The Dual Origin of Turtles from Pareiasaurs
“The origin of turtles (traditional clade: Testudines) has been a vexing problem in paleontology. New light was shed with the description of Odontochelys, a transitional specimen with a plastron and teeth, but no carapace. Recent studies nested Owenetta (Late Permian), Eunotosaurus (Middle Permian) and Pappochelys (Middle Triassic) as turtle ancestors with teeth, but without a carapace or plastron. A wider gamut phylogenetic analysis of tetrapods nests Owenetta, Eunotosaurus and Pappochelys far from turtles and far apart from each other. Here dual turtle clades arise from a clade of stem turtle pareiasaurs. Bunostegos (Late Permian) and Elginia (Late Permian) give rise to dome/hard-shell turtles with late-surviving Niolamia (Eocene) at that base, inheriting its Baroque horned skull from Elginia. In parallel, Sclerosaurus (Middle Triassic) and Arganaceras (Late Permian) give rise to flat/soft-shell turtles with Odontochelys (Late Triassic) at that base. In all prior phylogenetic analyses taxon exclusion obscured these relationships. The present study also exposes a long-standing error. The traditional squamosal in turtles is here identified as the supratemporal. The actual squamosal remains anterior to the quadrate in all turtles, whether fused to the quadratojugal or not.”

SVP abstracts – Are meiolaniform turtles stem turtles?

Kear et al. 2019 talk about
‘stem’ turtles with skull horns and club tails: the meiolaniforms.

From the abstract:
“Meiolaniforms (Meiolaniformes) are an enigmatic radiation of stem turtles with an exceptionally protracted 100 million-year evolutionary record that spans the mid-Cretaceous (Aptian–Albian) to Holocene. Their fossils have been documented for over 130 years, with the most famous examples being the derived Australasian and southern South American meiolaniids – bizarre horned turtles with massive domed shells and tail clubs that are thought to have been terrestrial and probably herbivorous.”

In the large reptile tree (LRT, 1592 taxa, subset Fig. 2) meiolaniforms (Fig. 1) are not enigmatic. They are basalmost hard-shell turtles derived from similarly-horned Elginia-type small pareiasaurs in parallel with Sclerosaurus-type small pareiasaurs basal to soft-shell turtles.

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

“Despite a long history of research, the phylogenetic affinities of meiolaniids have proven contentious because of ambiguous character state interpretations and incomplete fossils
representing the most ancient Cretaceous meiolaniform taxa.”

This problem is contentious only because of taxon exclusion. Prior workers have not included analyses of meiolaniforms and Elginia.

“Here, we therefore report the significant discovery of the stratigraphically oldest demonstrable meiolaniform remains, which were excavated from Hauterivian–Barremian high-paleolatitude (around 80°S) deposits of the Eumeralla Formation in Victoria, southeastern Australia. Synchrotron microtomographic imaging of multiple virtually complete skulls and shells provides a wealth of new data, which we combine with the most comprehensive meiolaniform dataset and Bayesian tip-dating to elucidate relationships, divergence timing and paleoecological diversity.”

Did the authors include Elginia, Sclerosaurus, Arganceras and Bunostegos? The abstract does not mention them.

“Our results reveal that meiolaniforms emerged as a discrete Austral Gondwanan lineage,
and basally branching sister group of crown turtles (Testudines) during the Jurassic.”

The LRT invalidated a monophyletic Testudines. Rather soft-shell and hard-shell turtles had separate parallel origins from within the small horned pareisaurs.

Figure 5. Subset of the LRT focusing on turtle origins and unrelated eunotosaurs.

Figure 5. Subset of the LRT focusing on turtle origins and unrelated eunotosaurs.

“We additionally recover a novel dichotomy within Meiolaniformes, which split into a unique Early Cretaceous trans-polar radiation incorporating apparently aquatic forms with flattened shells and vascularized bone microstructure, versus the larger-bodied terrestrial meiolaniids that persisted as Paleogene–Neogene relic species isolated in Patagonia and Australasia.”

That’s interesting. The LRT sort of separates the meiolaniform Niolama from the meiolaniform Meiolania + Proterochersis + Proganochelys. The latter taxon also has a club tail. Perhaps more meiolanforms would continue to nest with one or the other.

“Finally, our analyses resolve the paraphyletic stem of crown Testudines, which otherwise includes endemic clades of Jurassic–Cretaceous turtles distributed across the northern Laurasian landmasses. These had diverged from the Southern Hemisphere meiolaniforms by at least the Middle Jurassic, and thus parallel the vicariant biogeography of crown turtles, which likewise diversified globally in response to continental fragmentation and possibly climate.”

Outgroups are key to understanding turtle evolution in the LRT. So is taxon inclusion. Based on the dual origin of turtles from horned small pareiasaurs in the LRT, the list of stem turtles now includes pareiasaurs, if the concept of a monophyletic turtle still stands with a last common ancestor lacking a carapace and plastron within the pareiasaurs.


References
Kear BP et al. 2019. Cretaceous polar meiolaniform resolves stem turtle relationships. Journal of Vertebrate Paleontology abstracts.

Evolution of Sea Turtles video has no idea where turtles came from

 A new Ben Thomas video brings us old and invalid view on turtle origins.

I wrote in the comments section:
“Several traditional, but invalid hypotheses in this video. The ability to pull the head inside the shell, whether sideways or straight back is a highly derived character in the hardshell turtle lineage. Sea turtles and their ancestors never could do this. They branched off earlier. Only some soft shell turtles, like the Asian giant soft-shell turtle (Pelochelys) manage to pull half the skull inside a huge mass of scaly flesh by convergence. Eorhynchochelys is a giant eunotosaur. Both are derived from Acleistorhinus not close to turtles. Pappochelys is a basal sauropterygian, again not close to turtles. Sorry, Ben. Eunotosaurus details here:” http://www.reptileevolution.com/eunotosaurus.htm

“Hard shell and soft shell turtles had dual and parallel origins from the small, horned pareiasaurs Elginia and Sclerosaurus. We know turtle origins back to Silurian jawless fish. Cladogram of relationships that tests all published turtle origin candidates here: http://www.reptileevolution.com/reptile-tree.htm

No longer an enigma: Kudnu mackinlayi

I live for discoveries like this one,
which started as a Facebook post of the tiny specimen. This is what the LRT (Fig. 3) was built for.

Benton 1985 wrote:
“Bartholomai (1979) has described Kudnu [QMF8181], a partial snout from the early Triassic of Australia, as a paliguanid. The exact relationships of these forms to each other, and to other early ‘lizard-like’ forms are unclear (Carroll, 1975a, b, 1977; Currie, 1981c: 163-164; Estes, 1983: 12-15). Indeed, the group cannot be defined by any apomorphy, and the genera must be considered separately. As far as can be determined, all of these genera are lepidosauromorphs. Kudnu lacks the lepidosaur character X4 and the squamate character Y 1, but none of the others may be determined. Blomosaurus and Kudnu are classified here as Lepidosauromorpha, incertae sedis.”

Figure 1. Kudnu colorized using DGS and slight restored postcranially, shown 10x natural size at a 72 dpi standard screen resolution. Here's a taxon basal to Stephanospondylus, pareiasaurs and turtles. Prior workers excluded Stephanospondylus from their studies.

Figure 1. Kudnu colorized using DGS and slight restored postcranially, shown 10x natural size at a 72 dpi standard screen resolution. Here’s a taxon basal to Stephanospondylus, pareiasaurs and turtles. Prior workers excluded Stephanospondylus from their studies.

Contrad 2008 wrote:
“Other authors have followed this opinion and have described new ‘‘paliguanids’’, including Blomosaurus (Tatarinov, 1978) and Kudnu (Bartholomai, 1979). Even so, ‘‘Paliguanidae’’is widely regarded as a paraphyletic taxon and, unfortunately, the preservation of specimens constituting the known ‘‘paliguanid’’ genera (including Paliguana, Palaeagama, and Saurosternon) makes it impossible to characterize them except through plesiomorphy (Benton, 1985; Gauthier et al., 1988a; Rieppel, 1994). Thus, their position within Lepidosauromorpha is currently impossible to ascertain with any kind of precision.”

Evans and Jones 2010 wrote:
Kudnu (Australia, Bartholomai, 1979) and Blomosaurus (Russia, Tatarinov, 1978) are too poorly preserved to interpret with confidence but are probably also procolophonian.”

Figure 1. Click to enlarge. Stephanospondylus was considered a type of diadectid, but it nests with turtles and pareiasaurs, all derived from millerettids.

Figure 2.  Stephanospondylus was considered a type of diadectid, but it nests with turtles and pareiasaurs, all derived from millerettids,.. next to diadectids.

All that being said,
what does the LRT recover? In the large reptile tree (LRT, 1583 taxa, subset Fig. 3) Kudnu nests basal to Stephanospondylus (Fig. 2), a late survivor from deep in the lineage of pareiasaurs + turtles, not far from bolosaurids + diadectids + procolophonids. These clades are derived from Milleretta (Fig. 2) which was  2 to 3x larger.

Due to its small size,
Kudnu
can be considered phylogenetically miniaturized, the kind of taxon we often find at the base of many major reptile clades.

Sadly, earlier workers (see above)
were looking at the wrong candidates for sister taxa, excluding the right taxa. This is a problem that is minimized by the LRT due to its large number of taxa over a wide gamut.

Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

Figure 2. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.Figure 1. Carbonodraco enters the LRT alongside another recent addition, Kudnu, at the base of the pareiasaurs + turtles.

Once again,
you don’t need to see the fossil firsthand in a case like this. What you need is a wide gamut phylogenetic analysis like the LRT, to figure out how an enigma like Kudnu  nests with other reptiles.

If
Kudnu was earlier associated with Stephanospondylus, let me know and I will publish the citation. Otherwise, this is a novel hypothesis of interrelationships that inserts Kudnu without disturbing the rest of the LRT tree topology.


References
Bartholomai A 1979. New lizard-like reptiles from the Early Triassic of Queensland. Alcheringa: An Australasian Journal of Palaeontology 3:225–234.
Benton MJ 1985. Classification and phylogeny of the diapsid reptiles. Zoological Journal of the Linnean Society 84:97–164.
Conrad JL 2008. Phylogeny and systematics of Squamata (Reptilia) based on morphology.  Bulletin of the American Museum of Natural History 310: 182pp.
Evans SE and Jones MEH 2010. Chapter 2 The Origin, Early History and Diversification of Lepidosauromorph Reptiles in Bandyopadhyay S (ed.), New Aspects of Mesozoic Biodiversity, Lecture Notes in Earth Sciences 132, DOI 10.1007/978-3-642-10311-7_2 Springer-Verlag Berlin Heidelberg 2010

Did the turtle nuchal evolve from cleithra?

Lyson et al.  2013
propose a homology of the turtle nuchal (central anterior roof-like bone of the carapace) with the primitive cleithra (singular: cleithrum, slender, stem-like bone anterior to the scapula). In order to do so, they produced a set of turtle ancestors (or engineering models) that is not validated by the large reptile tree (LRT, 1395 taxa).

Frogs, lepidosaurs, diadectids and para-caseasaurs,
according to Lyson et al., model the ancestry of turtle shoulders and shells (Fig. 1).

Figure 1. On the left, from Lyson et al. 2013 with graphics added. On the right taxa basal to turtles according to the LRT.

Figure 1. On the left, from Lyson et al. 2013 with graphics added. On the right taxa basal to turtles according to the LRT. The right sequence documents a more gradual accumulation of traits. Even so, the gap between Bunostegos and Meiolania includes the complete development of the carapace and plastron… but almost everything else was present. A skull-only taxon, Elginia, nests between the two.

By contrast,
in the LRT Milleretta, is basal to Stephanospondylus, which is basal to diadectids on one branch and pareiasaurs, like Bunostegos, and the basal turtle Meiolania, on the other, documenting a more gradual accumulation of traits without introducing frogs and lepidosaurs. In the LRT, the gap between Bunostegos and Meiolania includes the unchronicled development of the carapace and plastron. Given that issue, almost everything else was present in the skeleton. A skull-only taxon, Elginia (not shown in Fig. 1), nests between the two. There is an online paper on turtle ancestors here.

Taxon exclusion is once again the problem.
Since Lyson et al. used inappropriate and unrelated taxa to demonstrate their hypothesis, it was invalid from the get-go. To my knowledge (let me know if I am wrong):

  1. No one recently suggested that frogs, like Rana, are basal to turtles.
  2. No one recently suggested that Diadectes is basal to turtles.
  3. No one recently suggested that Sphenodon is basal to turtles.
  4. Several authors (many from the Lyson et al. list) have suggested that Eunotosaurus was basal to turtles, but they did not test the above-listed LRT competing candidates when they published.

From Wikipedia Diadectidae
“Paleontologist E.C. Case compared diadectids to turtles in 1907, noting their large pectoral girdles, short, strong limbs, and robust skulls. Case described them as “lowly, sluggish, inoffensive herbivorous reptiles, clad in an armor of plate to protect them from the fiercely carnivorous pelycosaurs.”

The better method
for figuring out anything about turtles is to employ the valid ancestors of turtles, validated by testing against all other published candidates. I know, from testing, that all other candidates, like Eunotosaurus, nest far from turtles.

Getting back to our headline
and the title of the Lyson et al. paper, the genesis of the turtle carapace in hard-shell turtles is not preserved in the fossil record at present. Even so, the rarely preserved cleithrum gives little to no indication that it evolved into an anterior carapace bone… at present. Some day it may.

Lyson et al. note:
“unlike the other midline carapacial elements, the nuchal develops from paired mesenchymal condensations each of which contains a separate ossification center… first observed by Vallén (1942) and led him to conclude the nuchal was homologous with the supracleithra.”

The supracleithrum
by definition, “is a bone of the pectoral girdle situated dorsal to the cleithrum in some fishes and amphibians.”  That definition does not include reptiles.

If we look for a pre-nuchal in pareiasaurs
it is easy to find parasagittal osteoderms (Fig 2). Lyson et al. do not mention the word ‘pareiasaur’ in their paper.

Figure 2. The pareiasaur, Deltavjatia, with osteoderms in orange. Note the anterior set is simple and paired.

Figure 2. The pareiasaur, Deltavjatia, with osteoderms in orange. Note the anterior set is simple and paired, as hoped for by Lyson et al. but not found, except in turtle embryos, by Lyson et al.

Taxon exclusion can ruin a paper.
You can talk about thousands of characters for Eunotosaurus, but if you don’t include one pareiasaur, you’ll in the wrong ballpark on game day. Deltavjatia (Fig. 2) does not preserve a cleithrum. Rather, given its close, but not direct relation to turtles, the turtle nuchal likely arises from the osteoderms that are in place in Deltavjatia. They are the right size, in the correct orientation, and used for the same reason. So the nuchal probably arose from the foremost osteoderms on the torso, while those on the neck became neck armor. Remember, early turtles could not withdraw their neck.

It’s probably worthwhile to remind you of other body parts
that evolve in the ancestry of turtles until they become turtle traits at this time.

Figure 6. Turtle pelvis evolution. Here are the changes in the pelvis of pre-turtles and basal hard-shelled turtles.

Figure 3. Turtle pelvis evolution. Here are the changes in the pelvis of pre-turtles and basal hard-shelled turtles.

Take the turtle pelvis, for instance.
Similar precursors can be seen in stem turtle pareiasaurs (Fig. 3). And the skull is interesting. Workers have discussed Elginia with pareiasaurs and Meiolania with turtles, but never Meiolania with pareiasaurs or Elginia with turtles. That you heard here first in a three-part series five years ago.

Figure 2. Hard shell turtle evolution featuring Bunostegos, Elgenia, Meiolania and Proganochelys - NOT to scale.

Figure 4. Hard shell turtle evolution featuring the skulls of  Bunostegos, Elgenia, Meiolania and Proganochelys – NOT to scale. Note the long list of shared traits, longer than in any competing candidate.

If you know one of the seven authors
of Lyson et al. 2013, please make sure they become aware of this critique. A few of them are among those who rejected the submitted manuscript on the origin of turtles. Evidently they prefer the invalid status quo rather than this novel hypothesis for turtle origins.

References
Case EC 1907. Restoration of Diadectes. The Journal of Geology. 15 (6): 556–559.
Lyson TR, Bhullar B-AS, Bever GS, Joyce WG, de Queiroz K, Abzhanov A and Gauthier JA 2013. Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evolution & Development 15(5):317–325. DOI: 10.1111/ede.12041
Vallén E 1942. Beiträge zur Kenntnis der Ontogenie und der vergleichenden. Anatomie des Schildkrötenpanzers. Acta Zool. Stockholm 23: 1–127.

Resurrecting extinct taxa: Pareiasauria, Compsognathidae and Ophiacodontidae

Earlier we looked at
four clades thought to be extinct, but are not extinct based on their nesting in the large reptile tree (LRT, 1366 taxa). Today, three more:

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Figure 1. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Pareiasauria
According to Wikipedia, “Pareiasaurs (meaning “cheek lizards”) are an extinct group of anapsid reptiles classified in the family Pareiasauridae. They were large herbivores that flourished during the Permian period.”

In the LRT two clades of turtles (Fig. 1) are derived in parallel from two small horned pareiasaurs.

Figure 1. Lately the two clades based on two specimens of Compsognathus (one much larger than the other) have merged recently.

Figure 2.  Lately the two clades based on two specimens of Compsognathus (one much larger than the other) have merged recently.

Compsognathidae
According to Holtz 2004, “The most inclusive clade containing Compsognathus longipes but not Passer domesticsus.” Traditionally Compsognathus nests outside the Tyrannoraptora, a clade that traditionally leads to birds.

In the LRT Compsognathus specimens nest at the base of several theropod clades (Fig. 2) including the tyrannosaurs and Mirischia, Ornitholestes and the feathered theropods leading to birds.

Figure 1. Varanosaurus, Ophiacodon, Cutleria and Ictidorhinus. These are taxa at the base of the Therapsida. Ophiacodon did not cross into the Therapsida, but developed a larger size with a primitive morphology. This new reconstruction of Ophiacodon is based on the Field Museum (Chicago) specimen. Click to enlarge.

Figure  3. Varanosaurus, Ophiacodon, Cutleria and Ictidorhinus. These are taxa at the base of the Therapsida. Ophiacodon did not cross into the Therapsida, but developed a larger size with a primitive morphology. This new reconstruction of Ophiacodon is based on the Field Museum (Chicago) specimen. Click to enlarge.

Ophiacodontidae
According to Wikipedia, “Ophiacodontidae is an extinct family of early eupelycosaurs from the Carboniferous and Permian. Ophiacodontids are among the most basal synapsids, an offshoot of the lineage which includes therapsids and their descendants, the mammals. The group became extinct by the Middle Permian.”

In the LRT Ophiacodon (Fig. 3) and Archaeothyris, neither members of the Pelycosauria, are more directly related to basal therapsids, including derived the therapsids: mammals.

References
Holtz TR 2004. Basal tetanurae. PP. 71–110 in The Dinosauria, U of California Press.

/wiki/Pareiasaur
wiki/Ophiacodontidae

 

SVP 2018: Turtle ribs in softshell embryos

Hirasawa et al. 2018
studied the embryonic development of the Chinese soft-shell turtle, Pelodiscus sinensis, seeking clues to the origin of turtles.

Backstory:
The large reptile tree (LRT, 1313) tests a wide gamut of candidates, including all prior turtle ancestor candidates and a thousand more. It recovers a dual origin of turtles (hardshell and soft-shell) from two separate small horned pareiasaurs, Elginia and Sphodrosaurus.

Figure 2. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Figure 1. Another gap is filled by nesting E. wuyongae between Bunostegos and Elginia at the base of hard shell turtles in the LRT.

Hirasawa et al. report, “The turtles’ body plan differs from that of the other tetrapods in the solid dorsal and ventral shells (carapace and plastron).” Actually, no. The placodont Henodus has a similar carapace and plastron.

Hirasawa et al. report, “It has been widely accepted that the carapace and plastron evolved from the ribs and clavicular girdle plus gastralia, respectively, but the evolutionarytransition was poorly preserved in the fossil record.” In the LRT turtle ancestors did not have gastralia until the recent discovery that Sphodrosaurus was ancestral to soft-shell turtles and lateral (not medial) ‘gastralia’ (actually plastron progenitors) first appear.

FIgure 1. Partial reconstruction of Sphodrosaurus based on tracings in figure 2.

FIgure 2. Partial reconstruction of Sphodrosaurus based on tracings in figure 2. Plastron primordia appear in cyan (and so does the humerus and two sacrals, sorry!)

Hirasawa et al. report, “In the turtle embryo, the rib primordia are not extended to the lateral body wall unlike those of the other amniotes, and only the deep layer of the body wall muscle develops in the lateral body wall. Concomitantly, the sternum, which develops adjacent to the ventral ends of the ribs in the other amniotes, does not develop in the turtle embryo.” Actually the sternum is a rare ossification in tetrapods, not found in turtles, or LRT turtle ancestors. However the interclavicle is present in the turtle plastron.

Hirasawa et al. report, “Among fossil taxa, sauropterygians have repeatedly been placed in the closest position to turtles by phylogenetic analyses in previous studies.” In the LRT sauropterygians are not related to turtles except at the origin of the amnion in Viséan amphibian-like reptiles like Silvanerpeton.

The LRT is online for anyone to test taxa
relevant to the ancestry of turtles or any other included taxon or clade.

References
Hirasawa R et al. 2018. Developmental biological inferno on the evolution from the ribcage to the turtle shell. SVP abstract.