The Evolution of Unidirectional Pulmonary Airflow

Abstract

Conventional wisdom holds that the avian respiratory system is unique because air flows in the same direction through most of the gas-exchange tubules during both phases of ventilation. However, recent studies showing that unidirectional airflow also exists in crocodilians and lizards raise questions about the true phylogenetic distribution of unidirectional airflow, the selective drivers of the trait, the date of origin, and the functional consequences of this phenomenon. These discoveries suggest unidirectional flow was present in the common diapsid ancestor and are inconsistent with the traditional paradigm that unidirectional flow is an adaptation for supporting high rates of gas exchange. Instead, these discoveries suggest it may serve functions such as decreasing the work of breathing, decreasing evaporative respiratory water loss, reducing rates of heat loss, and facilitating crypsis. The divergence in the design of the respiratory system between unidirectionally ventilated lungs and tidally ventilated lungs, such as those found in mammals, is very old, with a minimum date for the divergence in the Permian Period. From this foundation, the avian and mammalian lineages evolved very different respiratory systems. I suggest the difference in design is due to the same selective pressure, expanded aerobic capacity, acting under different environmental conditions. High levels of atmospheric oxygen of the Permian Period relaxed selection for a thin blood-gas barrier and may have resulted in the homogeneous, broncho-alveolar design, whereas the reduced oxygen of the Mesozoic selected for a heterogeneous lung with an extremely thin blood-gas barrier. These differences in lung design may explain the puzzling pattern of ecomorphological diversification of Mesozoic mammals: all were small animals that did not occupy niches requiring a great aerobic capacity. The broncho-alveolar lung and the hypoxia of the Mesozoic may have restricted these mammals from exploiting niches of large body size, where cursorial locomotion can be advantageous, as well as other niches requiring great aerobic capacities, such as those using flapping flight. Furthermore, hypoxia may have exerted positive selection for a parasagittal posture, the diaphragm, and reduced erythrocyte size, innovations that enabled increased rates of ventilation and more rapid rates of diffusion in the lung.

The respiratory mechanics of the yacare caiman (Caiman yacareDaudine)

“…Recent research supports early suggestions that much of the lung of crocodilians may be relatively rigid and that airflow through the lung may be unidirectional, with posterior flow in the cervical ventral bronchus and its branches and anterior flow in the dorsobronchi and their branches during both lung inflation and deflation (Farmer, 2015). However, Claessens (2009) has shown that the lungs of Alligator mississippiensis may undergo large volume changes between maximal inspiration and expiration.…”

Low cost of pulmonary ventilation in American alligators (Alligator mississippiensis) stimulated with doxapram

“…Likewise, the consequences of the newly discovered unidirectional flow in the crocodilian lung (Farmer and Sanders, 2010;Farmer, 2015) for flow resistive forces may also be worthwhile considering for future analyses of the elastic versus non-elastic contributions to COV in crocodilians.…”

Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue

“…The diaphragm is not only critical for humans, but also for all mammals. The evolution of mammals involved the appearance of tidally ventilated, alveolar lungs and increased aerobic requirements (Farmer, 2015; Perry et al, 2010). It is thought that the evolution of the diaphragm in mammals was essential for obtaining maximal lung function, as the diaphragm both opens the thoracic cavity during inspiration (allowing for influx of air) and keeps the abdominal contents caudal.…”

“…How the diaphragm evolved at the origin of mammals during the Permian era is a major unanswered question (Farmer, 2015; Perry et al, 2010), but studies of diaphragm development in mouse suggest that the PPFs may be critical for diaphragm evolution. One way to elucidate the evolutionary origin of the diaphragm is to compare the developmental innovations present in mammals, but absent from birds and reptiles, which do not have a muscularized diaphragm.…”