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. 2018 Oct 24;5(10):180983.
doi: 10.1098/rsos.180983. eCollection 2018 Oct.

Vertebral Morphometrics and Lung Structure in Non-Avian Dinosaurs

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Free PMC article

Vertebral Morphometrics and Lung Structure in Non-Avian Dinosaurs

Robert J Brocklehurst et al. R Soc Open Sci. .
Free PMC article

Abstract

The lung-air sac system of modern birds is unique among vertebrates. However, debate surrounds whether an avian-style lung is restricted to birds or first appeared in their dinosaurian ancestors, as common osteological correlates for the respiratory system offer limited information on the lungs themselves. Here, we shed light on these issues by using axial morphology as a direct osteological correlate of lung structure, and quantifying vertebral shape using geometric morphometrics in birds, crocodilians and a wide range of dinosaurian taxa. Although fully avian lungs were a rather late innovation, we quantitatively show that non-avian dinosaurs and basal dinosauriforms possessed bird-like costovertebral joints and a furrowed thoracic ceiling. This would have immobilized the lung's dorsal surface, a structural prerequisite for a thinned blood-gas barrier and increased gas exchange potential. This could have permitted high levels of aerobic and metabolic activity in dinosaurs, even in the hypoxic conditions of the Mesozoic, contributing to their successful radiation.

Keywords: archosauria; axial skeleton; dinosauriformes; lung morphology; respiration.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Anatomy of the lung and thorax of extant archosaurs. (a) Dorsal view of the lungs and trachea of a hatchling American alligator (Alligator mississippiensis) generated from microCT. (b) Lungs of a hatchling A. mississippiensis in association with the vertebral column and dorsal ribs in left anterolateral view. (c) Interior of the thoracic cavity of A. mississippiensis with all viscera removed. (d) Dorsal view of the gas-exchanging lungs of the African grey parrot (Psittacus erithacus) (no air sacs are shown). (e) Lungs of P. erithacus in association with the vertebral column and dorsal ribs in left anterolateral view. (f) Interior of the thoracic cavity of the ostrich (Struthio camelus) with all viscera removed. Segmented surface models in (a,b,d,e) generated in the visualization programme Avizo 7.1 from microCT DICOM data of inflated lungs in situ. Abbreviation: s, costal sulci. Images not to scale.
Figure 2.
Figure 2.
The diapophysis, parapophysis and other vertebral landmarks. (ac) The six anterior-most dorsal vertebrae of (a) the extant crocodilian Crocodylus americanus (UMZC R6062), (b) the extant bird Struthio camelus (NMS 1879.85.9) and (c) the extinct theropod Allosaurus fragilis (Madsen, 1976 [41]) showing the positions of the parapophysis (pink) and the diapophysis (blue). (d) Landmarks used to quantify vertebral shape variation in archosaurs, shown on the first dorsal vertebra of Crocodylus americanus (UMZC R6062). For detailed descriptions of each landmark, see the electronic supplementary material.
Figure 3.
Figure 3.
Principal components analysis. (a) Vertebral morphospace produced by PCA of the entire dataset. Shape graphs represent extremes of each PC axis. (be) Vertebrae from individual fossil groups compared with extant groups. Each point represents one vertebra. Taxa colour coded by taxonomic group.
Figure 4.
Figure 4.
Linear discriminant analysis. (a) Vertebral morphospace produced using LDA. Linear discriminant scores are generated using the extant dataset; then, the linear discriminant scores are used to estimate the position of fossil taxa in this space. Shape graphs represent extremes of each LD axis. (be) Vertebrae from individual fossil groups compared with extant groups. Each point represents one vertebra. Taxa colour coded by taxonomic group.
Figure 5.
Figure 5.
Shape variation along the vertebral column. (a) Vertebral number plotted against the linear discriminant 1 score. (b) Same, but with vertebral number normalized according to the total number of dorsal vertebrae in each taxon. Taxa colour coded by taxonomic group.
Figure 6.
Figure 6.
Shape variation across phylogeny. An informal supertree of the taxa used in this study, with the range and mean of the linear discriminant 1 scores for the whole vertebral column plotted for each taxon in the phylogeny. Taxa colour coded by taxonomic group. The red band represents the range of values seen in extant birds.
Figure 7.
Figure 7.
Evolution of the archosaur respiratory system. A phylogeny of Archosauria, showing key modifications to the respiratory system associated with the evolution of the avian lung-air sac system.

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  • The evolution of mechanisms involved in vertebrate endothermy.
    Legendre LJ, Davesne D. Legendre LJ, et al. Philos Trans R Soc Lond B Biol Sci. 2020 Mar 2;375(1793):20190136. doi: 10.1098/rstb.2019.0136. Epub 2020 Jan 13. Philos Trans R Soc Lond B Biol Sci. 2020. PMID: 31928191
  • Comment on Brocklehurst et al.
    Paul G. Paul G. R Soc Open Sci. 2019 Feb 27;6(2):181872. doi: 10.1098/rsos.181872. eCollection 2019 Feb. R Soc Open Sci. 2019. PMID: 30891298 Free PMC article. No abstract available.

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