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

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.Energetically demanding forms of locomotion, such as powered flight, require a great capacity for gas exchange and selection for aerobic stamina may underlie many unique features of the avian respiratory system (1, 2). The avian respiratory system consists of highly vascularized lungs and avascular air sacs, which are membranous structures that effect ventilation and, in some species, extend between the muscles and even enter the bones (3). The topography of the conducting airways is complex; they form a circular system of tubes, analogous to the loop formed by the blood circulatory system in which arteries connect to veins through numerous small diameter vessels, the capillaries. Likewise, the avian conducting airways connect to each other through numerous tubules, the parabronchi, to form a circular path for respiratory gases (3). Gases flow through most of the parabronchi in the same direction during both inhalation and exhalation (unidirectional flow). This is due to the presence of aerodynamic valves (4–10). In contrast, the mammalian conducting airways arborize with the branch tips ending in blind sacs, there are no valves, and gases travel in the opposite direction along the conducting airways during expiration from the direction followed during inspiration (tidal flow). The presence of aerodynamic valves and unidirectional flow has generally been thought to be a highly derived feature found, among extant animals, only in birds and having evolved either in the crown group with flight or somewhere along the saurischian lineage leading to birds (11), perhaps as a mechanism to meet the high energetic demands of endothermy.The discovery of unidirectional flow in the lungs of alligators (12, 13) and the savannah monitor lizard (14) indicates that we do not understand the distribution of this phenomenon among different lineages of vertebrates and raises questions about its underlying value. It is possible that unidirectional flow evolved convergently in crocodilians and monitor lizards and serves to expand aerobic capacity. Although monitor lizards are ectotherms, their lifestyles are largely convergent with small predatory mammals (15) and they have high aerobic capacities compared with other lizards (16). In contrast, extant alligators have limited aerobic stamina (17) but their common ancestor with birds may have had a great aerobic capacity (18) or may have been endothermic (19, 20). Crocodilians and monitor lizards also share a suite of features of their pulmonary and cardiac anatomy that have been purported to give rise to, or coevolve with, birdlike patterns of flow. These features are: (i) a bronchus that has grown deep into the lung as a mesobronchium, (ii) partitioning of the respiratory system into a mechanical part that functions in ventilation and a gas-exchanging region, (iii) intercameral perforations, and (iv) separation of the heart into right and left sides (1, 21). Crocodilians and monitors are also derived in having evolved mechanisms to supplement costal ventilation while exercising (18, 22, 23). Thus, unidirectional flow in these lineages may be one of many derived traits underpinning exceptionally high rates of oxygen consumption during activity.It is also possible, however, that this pattern of flow evolved before the split of Diapsida into the Lepidosauromorpha (tuatara, lizards, snakes) and Archosauromorpha (crocodilians and birds) in an ectothermic ancestor lacking expanded aerobic capacities and living as long ago as the Permian Period. Unidirectional flow has been purported to serve ectotherms by harnessing the heart as a pump for air during periods of breath-holding (apnea) (12). Light can be shed on this pattern of evolution with observations of more squamates (snakes, lizards), which are the most diverse and largest (∼9,000 species) group of living reptiles (24).To test the hypothesis that unidirectional flow is present in squamates other than varanid lizards; to better understand anatomical features that give rise to these patterns of flow; and to gain insight into the underlying value of this pattern of flow, green iguanas (Iguana iguana) were studied. Green iguanas differ from monitors because they are herbivores and because they have structurally simple lungs that lack an enclosed intrapulmonary bronchus. Iguanas lack septation of the cardiac ventricle and have poor locomotor stamina. The poor stamina is due in part from an impairment during running in their blood and air circulatory systems (19, 25, 26).