The absence of an invasive air sac system in the earliest dinosaurs suggests multiple origins of vertebral pneumaticity

Abstract

The origin of the air sac system present in birds has been an enigma for decades. Skeletal pneumaticity related to an air sac system is present in both derived non-avian dinosaurs and pterosaurs. But the question remained open whether this was a shared trait present in the common avemetatarsalian ancestor. We analyzed three taxa from the Late Triassic of South Brazil, which are some of the oldest representatives of this clade (233.23 ± 0.73 Ma), including two sauropodomorphs and one herrerasaurid. All three taxa present shallow lateral fossae in the centra of their presacral vertebrae. Foramina are present in many of the fossae but at diminutive sizes consistent with neurovascular rather than pneumatic origin. Micro-tomography reveals a chaotic architecture of dense apneumatic bone tissue in all three taxa. The early sauropodomorphs showed more complex vascularity, which possibly served as the framework for the future camerate and camellate pneumatic structures of more derived saurischians. Finally, the evidence of the absence of postcranial skeletal pneumaticity in the oldest dinosaurs contradicts the homology hypothesis for an invasive diverticula system and suggests that this trait evolved independently at least 3 times in pterosaurs, theropods, and sauropodomorphs.

Figure 1

Examples of vertebrae with apneumatic (A–F) and pneumatic (G–L) architectures, and schematic drawings of vertebral fossae and laminae in (M and N). (A,B) Varanus komodoensis (NHMUK RR 1934.9.2.2). (C,D) Alligator mississippiensis (OUVC 11415 and NHMUK RR 1975.14.23, respectively). (E) Odocoeileus virginianus. (F) Bos taurus. (G,H) Apatosaurus sp. (MOR 957 6-29-92). (I,J) noasauridae indet. (DGM 929-R). (K,L) Ibirania parva (LPP-PV-0200). (M,N) Dilophosaurus wetherilli. Lateral view in (A,C,F,I,L,N). Transverse sections in (B,D,E,J,K,M). Ventral view in (G). High contrast outlines in A-D and G-L based on CT scan data. (M and N) are based on the original schematic drawing of Adam Marsh. WitmerLab at Ohio University provided access to the Alligator data originally appearing on their website, the collection of which was funded by NSF. The file was downloaded from www.MorphoSource.org, Duke University. Not to scale. Figures were generated with Adobe Illustrator CC version 22 X64.

Figure 2

Detail of the vertebrae and foramina of the basalmost sauropodomorph Buriolestes (CAPPA/UFSM-0035). Cervical (A–C), anterior (D–F) and posterior (G–I) dorsal vertebrae in right lateral view. Note that nutritional foramina are present throughout the axial skeleton (dark arrows). Anterior/posterior orientation was defined based on the axial position, not the anatomical plane. Scale bar = 5 mm. Figures were generated with Adobe Photoshop CC version 22.5.1 X64.

Figure 3

Detail of the vertebrae and foramina of the early sauropodomorph Pampadromaeus (ULBRA-PV016; (A,B)) and the herrerasaurid Gnathovorax (CAPPA/UFSM-0009; (C–F)). Anterior dorsal vertebrae in (A,B). Anterior cervical in C and posterior cervical in (D–F). Nutritional foramina are present on the lateral surface of the centra (small arrows) in (A,B) and (D–F. They present a diminutive diameter when located inside the lateral fossae (D–F) and are broader on the ventral portion of the centra (C). Scale bar in (A,B) = 5 mm; in (C–E) = 1 mm; in (F) = 0.1 mm. Figures were generated with Adobe Photoshop CC version 22.5.1 X64.

Figure 4

Micro-computed tomography of the vertebrae of the basalmost sauropodomorph Buriolestes (CAPPA/UFSM 0035). (A) silhouette shows the position of the axial elements. Artist: Felipe Elias. (B), three-dimensional reconstruction of the articulated cervical vertebral series and the correspondent high-contrast density slices in (D–I). Diagenetic processes partially compromised the internal structures in these cervicals. (C), 3D reconstruction of the articulated anterior dorsal vertebrae and the correspondent high-contrast density slices in (J–M). Small circumferential chambers occur both ventrally in the dorsal centrum (J) and laterally in the neural arch pedicles (D). All images indicate apneumatic chaotic trabeculae architecture. Some of the latter develop into larger chambers in the centrum (E,J,K). Nutritional foramina are broader at the bottom of the neural canal in the posterior cervicals (F,G). All slices were taken from the approximate midshaft. Anterior views in (D–H,J,K). Lateral view in (L). Ventral view in (H,I,M). Anterior/posterior orientation was defined based on the axial position, not the anatomical plane. cc circumferential chamber, ccv chamber in the centrum, ctr chaotic trabecula, d diapophysis, ltr layered trabeculae, nc neural canal, nf nutritional foramen, s neural spine. Scale bar in (A) = 500 mm; in (B–M) = 10 mm. Computed tomography data processed with 3D Slicer version 4.10. Figures were generated with Adobe Photoshop CC version 22.5.1 X64.

Figure 5

Micro-computed tomography of the vertebrae of the herrerasaurid Gnathovorax (CAPPA/UFSM-0009). (A) silhouette shows the position of the axial elements. Artist: Felipe Elias. (B) 3D reconstruction of the anterior cervical vertebra and the correspondent high-contrast density slices in (D-I). Diagenetic artifacts greatly compromised the internal structures. (C) 3D reconstruction of the articulated posterior cervical vertebrae and the correspondent high-contrast density slices in (J–O). Minerals infilled between trabecular vacancies generate reddish anomalies. All images indicate irregular, chaotic, apneumatic architecture. Note the apneumatic large chambers in the centrum (ccv) and the smaller circumferential chambers at the bottom (cc). All slices were taken from the approximate midshaft. Anterior views in (D,H,I). Right lateral view in (E,L,M). Ventral view in (F,G,J,K). cc circumferential chambers, ccv chamber in the centrum, ce centrum, ctr chaotic trabeculae, d diapophysis, dia diagenetic artifact, nc neural canal, nf nutritional foramen, poz postzygapophysis, prz prezygapophysis. Scale bar in (A) = 1000 mm; in (B–O) = 10 mm. Computed tomography data processed with 3D Slicer version 4.10. Figures were generated with Adobe Photoshop CC version 22.5.1 X64.

Figure 6

Micro-computed tomography of the vertebrae of the early sauropodomorph Pampadromaeus (ULBRA-PV016). (A) silhouette shows the position of the axial elements. Artist: Felipe Elias. (B) 3D reconstruction of the mid-dorsal vertebra and the correspondent high-contrast density slices in (D–G). Diagenetic artifacts significantly compromised the internal structures in this element. (C) 3D reconstruction of the articulated anterior dorsal vertebrae and the correspondent high-contrast density slices in (H–M). Note the circumferential chambers at the bottom of the centrum in (H). Also, note the ‘pseudopolycamerate’ architecture in (L). All images indicate irregular, chaotic, apneumatic architecture. All slices were taken from the approximate midshaft. Anterior views in (D,H,I). Right lateral view in (E,L,M). Ventral view in (F,G,J,K). cc circumferential chambers, ce centrum, ctr chaotic trabeculae, d diapophysis, dia diagenetic artifact, ltr layered trabeculae, nc neural canal, nf nutritional foramen, ppc ‘pseudopolycamerate’ architecture, prz prezygapophysis. Scale bar in (A) = 500 mm; in (B–M) = 10 mm. Computed tomography data processed with 3D Slicer version 4.10. Figures were generated with Adobe Photoshop CC version 22.5.1 X64.

Figure 7

Schematic profile of the internal architecture of two saurischians. (A) Dilophosaurus, showing a polycamerate pneumatic structure. (B) Pampadromaeus, demonstrating pseudo-polycamerate apneumatic trabeculae. (A) is based on Marsh and Brum et al.. Not to scale. Figures were generated with Adobe Illustrator CC version 20 X64.

Figure 8

A simplified cladogram of Avemetatarsalia illustrates the branches in which the unambiguous presence of an air sacs system has been evidenced (bright/green ‘check’ sign). The absence of an air sacs system in the oldest dinosaurs presented in this study eliminates the hypothesis of the homology of this trait between pterosaurs and saurischians. Our results also corroborate that this trait appeared independently in three clades: Pterosauria, Theropoda, and Sauropoda. “Early Sauropodomorpha” is a paraphyletic branch. Cladogram based on Novas et al.. Silhouettes authored by Felipe Elias, Scott Hartman, Tasman Dixon, Jagged Fang, and FunkMonk. Figures were generated with Corel Draw X6 version.