Unidirectional pulmonary airflow patterns in the savannah monitor lizard

Unlike the tidal (in and out) breathing of mammals, bird lungs have unidirectional airflow patterns; here the savannah monitor lizard is shown to have unidirectional airflow too, with profound implications for the evolution of unidirectional airflow in reptiles, predating the origin of birds. Ventilation in mammals is tidal — breathe in then breathe out. In birds, however, the situation is more complicated. The lungs are just part of an extensive network of air sacs connected in such a way that airflow is unidirectional. It was thought that this arrangement was related to the energetic demands of flight but when similar systems were found in crocodilians and inferred in dinosaurs, it appeared that unidirectional airflow ventilation may have been primitive for archosaurs — the clade that includes birds, crocodiles and dinosaurs. But could the unidirectional airflow system be even more widespread? Lepidosaurs (lizards, snakes and allies) are the sister taxon to archosaurs and now a study of the monitor lizard shows that for this lepidosaur, at least some of its ventilation is tidal. This is an important discovery, but the jury is still out on whether unidirectional airflow is a convergent feature of archosaurs and lepidosaurs, or whether it is a basal character of both groups. If the latter, then unidirectional airflow evolved 100 million years before the first bird flew. 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.