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New insight into the evolution of the vertebrate respiratory system and the discovery of unidirectional airflow in iguana lungs

Significance The avian respiratory system appears strikingly distinct from all other animals. Purported key innovations underpinning avian patterns of airflow are an enclosed intrapulmonary bronchus, intercameral perforations, heterogeneous parenchyma; these traits allegedly coevolved with separation of the cardiac ventricle into right and left sides and are presumed to have been favored by selection because they facilitate high activity metabolisms. In contradistinction to these prevailing theories, here we show that unidirectional flow is present in the lungs of the green iguana, an ectothermic animal with low aerobic capacity, no intrapulmonary bronchus, and no intercameral perforations. This discovery indicates a transformation in our understanding of the evolution of the vertebrate respiratory system is needed. The generally accepted framework for the evolution of a key feature of the avian respiratory system, unidirectional airflow, is that it is an adaptation for efficiency of gas exchange and expanded aerobic capacities, and therefore it has historically been viewed as important to the ability of birds to fly and to maintain an endothermic metabolism. This pattern of flow has been presumed to arise from specific features of the respiratory system, such as an enclosed intrapulmonary bronchus and parabronchi. Here we show unidirectional airflow in the green iguana, a lizard with a strikingly different natural history from that of birds and lacking these anatomical features. This discovery indicates a paradigm shift is needed. The selective drivers of the trait, its date of origin, and the fundamental aerodynamic mechanisms by which unidirectional flow arises must be reassessed to be congruent with the natural history of this lineage. Unidirectional flow may serve functions other than expanded aerobic capacity; it may have been present in the ancestral diapsid; and it can occur in structurally simple lungs.