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

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