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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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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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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Related audio
41586_2014_BFnature12871_MOESM6_ESM.mp3 (download 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 (download MP4 )
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 (download MP4 )
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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DOI: https://doi.org/10.1038/nature12871
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CG Farmer
I would like to start a discussion on the history of the discovery of unidirectional airflow in lungs by acknowledging Matt Wedel and Heinrich Mallison for bringing into the limelight a publication by S. Wolf (1933)<sup>1</sup>. It is a pity that much of the classical literature remains untranslated, and in consequence many of the seminal ideas, whether ultimately found to be correct or not, are not cherished. My coauthors and I are therefore grateful to Heinrich for offering to translate papers from German to English. This is no doubt time-consuming work and his willingness to contribute in this way speaks volumes about his commitment to keeping this older literature from being forgotten. Below is a summary of Mallison?s translation of Wolf, which is germane to our publication on unidirectional airflow in the savannah monitor lizard.
Wolf?s publication is a detailed study on the lungs of non-avian reptiles that focuses on his experimental work on turtles. However he also discusses lizards, snakes, and birds. Wolf, and perhaps others before him, discussed the possibility of birdlike lungs in non-avian reptiles. Wolf stated that the construction of a birdlike lung required three things: 1) the separation of the lung into ventilatory and respiratory parts; 2) the presence of an intrapulmonary bronchus that grows deep into the lung as a mesobronchium so that air can be steered to the caudal ventilatory part; 3) the formation of communications that let the air move from the ventilatory part through the respiratory part like the saccobronchi of birds, rather than traveling back through the intrapulmonary bronchus. He furthermore stated, based on the work of Beth, Brandes, and Dotterweich, that air was steered in bird lungs by rings of muscle that served as mechanical valves. Because he thought that the bird lung was especially good at ?efficiently exploiting? oxygen and that this is mandatory for flight, he suggested that similarities to the bird lung might be found in groups of non-avian reptiles that had high demands placed on their respiratory systems and that they would be found in the same clades that had modifications of the cardiovascular system that "progressed" them toward a four chambered heart.
Wolf stated that many reptiles have caudal and cranial saccular regions of the respiratory system with the gas-exchange parenchyma concentrated medially, fulfilling his first criterion for the avian lung. Furthermore, he believed that he had found evidence of mechanical valves in lizard lungs because insufflation of dissected lungs resulted in air remaining in the lungs even though the trachea was not sealed (Tiliqua of uncertain species). He also noted that an intrapulmonary bronchus was present in some groups (e.g., Lacerta ocellate, Scincus officinalis, varanids, crocodiles, chelonians, some snakes), and he speculated that in these groups the inhaled air would pass entirely, or at least in large part, to the caudal ventilatory part, fulfilling his second criterion. Finally, Wolf stated that in monitor lizards and some snakes, there are air passages that are functionally comparable to the saccobronchi, so that air could move from the caudal ventilatory part to the respiratory part without flowing back into the intrapulmonary bronchus. Milani illustrated a monitor lung without showing these connections, which Wolf thought was erroneous, and to prove these connections existed Wolf put a small amount of water into the lung and observed that it moved into the caudal end when that end was tilted down establishing a lateral path for flow from cranial to caudal end. From these observations Wolf suggested that it was possible that monitors and some snakes (e.g., Eunectes murinus) shunted air like birds. His discussion of turtles is more thorough but less clear to me.
Wolf noted that chelonians have rather long bronchi that are remarkable for their cartilaginous support and that the caudal regions of the lung contain little vasculature. He furthermore noted that there are ?reverse connections? to the respiratory part of the lung and claimed that respired air does not emanate from the caudal chamber, with the exception of Trionyx; in this clade he proposed the caudal chamber was strongly perfused with blood and functioned in gas exchange. However, when Wolf put live specimens of Emys europaea under a solution of eosin at various orientations (head up or down or obliquely inclined, in prone and supine positions) he never saw the inhaled solution reach the caudal chambers, in contradiction to his hypothesis that enclosed intrapulmonary bronchi cause fluid to flow directly to the caudal regions of the lung. Wolf also subjected turtles to various regimens of flow while they were submerged to determine the time it takes before they succumb to drowning and concluded the animals were using means other than the lungs for gas exchange. To rule out the use of the anal sacs for respiration, Wolf sutured shut the anal orifice with no adverse effects on dive duration. Wolf proposed cutaneous respiration was of great importance, and to show this he painted the non-plated and plated parts of the animal with collodion to bereave them of respiration. Wolf pointed out that in the lungs of Emys and Testudo, saccobonchi-like communications are missing and that it is not impossible that these sorts of communications are present in giant and marine tortoises. Although many of Wolf's experiments are horrific when viewed from today's standards of ethical treatment of animal subjects, he did ask a number of interesting questions.
	Our studies on lung structure-function relationships of reptiles have not been guided by Wolf?s publication, although our study on savannah monitors shows he was right about birdlike patterns of flow in these animals. However I believe he was right for the wrong reasons. I do not think any of the three criteria he lists as requisite for birdlike patterns of flow are needed to produce unidirectional airflow. I think it is possible to have such flow in animals that lack separation of the respiratory system into gas-exchange and ventilatory regions and that furthermore lack enclosed intrapulmonary bronchi and intercameral perforations. Our current understanding of lung structure-function relationships does not corroborate Wolf?s theory that the bird lung arose to support high metabolic demands (flight). The excellent work of J. Maina has detailed how the broncho-alveolar lungs of bats are very capable of supporting flight. It is now widely accepted that, contrary to Wolf, there are no muscular valves steering airflow in the bird lung and our data showing that unidirectional flow persists in excised lungs of crocodilians and monitor lizards indicates that muscular valves are not required in these lineages either. Finally, I do not think these traits co-evolved with separation of the cardiovascular system into right and left sides in sauropsids. It is difficult to deduce patterns of flow from anatomy alone because fluid flow can be counterintuitive, as the superb work of S. Vogel, E. Hazelhoff, and others have shown. Thanks to modern computational and other methodologies we are able to probe these age-old questions with new rigor, insight, and depth, which makes this a very exciting time to study lung evolution.
1	Wolf, S. Zur kenntnis von Bau und Funktion der Reptilienlunge. Zool. Jahrb. Abt. Anat. Ontol. 57, 139-190 (1933).