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Unidirectional pulmonary airflow patterns in the savannah monitor lizard

Nature volume 506, pages 367–370 (2014)Cite this article

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Abstract

The unidirectional airflow patterns in the lungs of birds have long been considered a unique and specialized trait associated with the oxygen demands of flying, their endothermic metabolism1 and unusual pulmonary architecture2,3. However, the discovery of similar flow patterns in the lungs of crocodilians indicates that this character is probably ancestral for all archosaurs—the group that includes extant birds and crocodilians as well as their extinct relatives, such as pterosaurs and dinosaurs4,5,6. Unidirectional flow in birds results from aerodynamic valves, rather than from sphincters or other physical mechanisms7,8, and similar aerodynamic valves seem to be present in crocodilians4,5,6. The anatomical and developmental similarities in the primary and secondary bronchi of birds and crocodilians suggest that these structures and airflow patterns may be homologous4,5,6,9. The origin of this pattern is at least as old as the split between crocodilians and birds, which occurred in the Triassic period10. Alternatively, this pattern of flow may be even older; this hypothesis can be tested by investigating patterns of airflow in members of the outgroup to birds and crocodilians, the Lepidosauromorpha (tuatara, lizards and snakes). Here we demonstrate region-specific unidirectional airflow in the lungs of the savannah monitor lizard (Varanus exanthematicus). The presence of unidirectional flow in the lungs of V. exanthematicus thus gives rise to two possible evolutionary scenarios: either unidirectional airflow evolved independently in archosaurs and monitor lizards, or these flow patterns are homologous in archosaurs and V. exanthematicus, having evolved only once in ancestral diapsids (the clade encompassing snakes, lizards, crocodilians and birds). If unidirectional airflow is plesiomorphic for Diapsida, this respiratory character can be reconstructed for extinct diapsids, and evolved in a small ectothermic tetrapod during the Palaeozoic era at least a hundred million years before the origin of birds.

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Figure 1: Pulmonary anatomy and airflow patterns of Varanus exanthematicus.
Figure 2: Airflow recorded in vivo.
Figure 3: Phylogeny for Diapsida showing lungs of representative taxa.

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Acknowledgements

We thank J. Dix (Reptile Rescue Service) for the donation of deceased varanid specimens, J. Bourke for assistance with Avizo, and D. Shafer for German translations. This work was supported by an American Association of Anatomists Postdoctoral Fellowship and an American Philosophical Society Franklin Research Grant to E.R.S., National Science Foundation grants to C.G.F. (IOS-1055080 and IOS-0818973) and a generous donation to the Farmer laboratory by S. Meyer.

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Authors and Affiliations

  1. Department of Biology, University of Utah, Salt Lake City, 84112, Utah, USA

    Emma R. Schachner, Robert L. Cieri & C. G. Farmer

  2. Division of Sleep Medicine, Department of Medicine, Harvard Medical School, Boston, 02215, Massachusetts, USA

    James P. Butler

  3. Department of Environmental Health, Molecular and Integrative Physiologic Science Program, Harvard School of Public Health, Boston, 02115, Massachusetts, USA

    James P. Butler

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  1. Emma R. Schachner
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  4. C. G. Farmer
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Contributions

E.R.S. and R.L.C. conducted the in vivo surgeries. All authors collected data on excised lungs. E.R.S. acquired the CT scans and generated the three-dimensional digital models. C.G.F. and J.P.B. supervised and contributed ideas throughout the project. All authors contributed to the manuscript.

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Correspondence to Emma R. Schachner or C. G. Farmer.

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The authors declare no competing financial interests.

Related audio

41586_2014_BFnature12871_MOESM6_ESM.mp3

Some lizards breathe like birds, using a one-way system to get air through their bodies. Research Emma Schachner explains what that means for evolution.

Supplementary information

3D model of the skeletal and pulmonary anatomy of Varanus exanthematicus

A volume rendered three dimensional skeleton and segmented surface of the lungs and bronchial tree (left craniolateral view) of a female Varanus exanthematicus generated from a CT scan. The bronchus in which in vivo unidirectional flow was measured is indicated. Abbreviations: cb, cervical bronchus; L1-L10, lateral bronchi 1-10; M1-M11, medial bronchi 1-11. (MP4 29060 kb)

Unidirectional movement of fluid through regions of the lung in V. exanthematicus

Microsphere infused saline flowing from lateral bronchus 10 to lateral bronchus 9 in an excised right lung during manual ventilation (60 cc syringe). The microspheres can be seen moving from right to left (caudal to cranial) during inspiration and expiration. Abbreviations: L9, lateral bronchus 9; L10, lateral bronchus 10. (MP4 27392 kb)

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Schachner, E., Cieri, R., Butler, J. et al. Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature 506, 367–370 (2014). https://doi.org/10.1038/nature12871

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