Evolution of Unidirectional Pulmonary Airflow

Conventional wisdom has held that birds are unique in having a bronchial tree that foms a circuit through which gases move in the same direction during both phases of ventilation. This unidirectional flow is caused by aerodynamic, as opposed to mechanical valves. Unidirectional airflow combined with either crosscurrent or countercurrent gas exchange has been thought to be important for expanding aerobic capacity, a trait that is essential for sustaining aerobically demanding forms of locomotion, such as flapping flight. In contrast, airflow through the mammalian bronchial tree is tidal and this has generally been thought to be true for other vertebrates. However, undirectional flow occurs in crocodilians and iguanid and monitor lizards, suggesting unidirectional flow is much older and much more widespread than previously believed, and is perhaps useful for ectothermic groups that have a low energy life history. These discoveries raise questions about the selective drivers and functional significance of unidirectional flow, and transform our understanding of the evolution of this phenomenon.

Schematic of airflow in the avian lung During inspiration the airsac expand and air flows into the bird. In the lung, part of the stream of fresh air (red) flows directly through the intrapulmonary bronchus and into the caudal air sacs and part flows into the dorosbronchi, through the parabronchi, into the ventrobornchi, and finally into the cranial airsacs. On expiration, the air in the caudal air sacs flows into the dorso, para, and ventrobronchial circuit before leaving the lung by way of the primary bronchus (after Wang et al 1992).	Computed tomography and map of airflow in the alligator lung Airflow through the homologues of the avian dorso bronchi (blue, yellow, red) and the ventrobronchi (geen), and parabronchi (dashed lines) is in the same direction during both phases of ventilation. The region of the lung that lies ventrocaudal to the conducting airways is homologous to the avian air sacs. Arrows show directiong of airflow (based on Farmer and Sanders 2010, Farmer 2010).
Computational Fluid Dynamics Model of Airflow in the Green Iguana A) Medial view of volumetric mesh generated from computed tomography data. Head is toward the left. Flow during two differeint times inspiration (B and C) and expiration (D and E) is projected in the coronal (left) and axial (right) planes. Along the mesial wall the flow is undirectional and moves craniad (red color). During inspiration there is a high speed stream moving caudad along part of the lateral wall (from Cieri et al 2014)	Schematic of airflow in the monitor lung Air flows cranaid along the lateral wall during both phases of ventilation (from Schachner et al. 2014).

Schematic of airflow in the avian lung

During inspiration the airsac expand and air flows into the bird. In the lung, part of the stream of fresh air (red) flows directly through the intrapulmonary bronchus and into the caudal air sacs and part flows into the dorosbronchi, through the parabronchi, into the ventrobornchi, and finally into the cranial airsacs. On expiration, the air in the caudal air sacs flows into the dorso, para, and ventrobronchial circuit before leaving the lung by way of the primary bronchus (after Wang et al 1992).

Computed tomography and map of airflow in the alligator lung

Airflow through the homologues of the avian dorso bronchi (blue, yellow, red) and the ventrobronchi (geen), and parabronchi (dashed lines) is in the same direction during both phases of ventilation. The region of the lung that lies ventrocaudal to the conducting airways is homologous to the avian air sacs. Arrows show directiong of airflow (based on Farmer and Sanders 2010, Farmer 2010).

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Computational Fluid Dynamics Model of Airflow in the Green Iguana

A) Medial view of volumetric mesh generated from computed tomography data. Head is toward the left. Flow during two differeint times inspiration (B and C) and expiration (D and E) is projected in the coronal (left) and axial (right) planes. Along the mesial wall the flow is undirectional and moves craniad (red color). During inspiration there is a high speed stream moving caudad along part of the lateral wall (from Cieri et al 2014)

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Schematic of airflow in the monitor lung

Air flows cranaid along the lateral wall during both phases of ventilation (from Schachner et al. 2014).

Farmer, CG. 2016. Similarity of crocodilian and avian lungs indicates unidirectional flow is ancestral for archosaurs. Integrative and Comparative Biology 55 (6): 1-10. PDF

Farmer, CG. 2015. The evolution of unidirectional pulmonary airflow. Physiology 30: 260-272. PDF

Cieri, R., Farmer, CG. 2015. Unidirectional pulmonary airflow in vertebrates: a review of structure, function, and evolution. Journal of Comparative Physiology B 186 (5): 541-552. PDF

Cieri, R., Craven, B., Schachner, E., Farmer, CG. 2014. New insight into the evolution of the vertebrate respiratory system and the discovery of unidirectional airflow in iguanan lungs. PNAS 111 (48) 17218-17223. PDF Supplemental data PDF

Schachner, E.R., Cieri, R. Butler, J., Farmer, CG. 2014. Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature 506: 367-370. PDF

Farmer, CG and K Sanders. 2010. Unidirectional airflow in the lungs of alligators. Science. 327:338-340 PDF Supplemental data PDF

Farmer, CG. 2010. The provenance of the alveolar and parabronchial lungs: Insights from paleoecology and the discovery of cardiogenic, unidirectional airflow in the American alligator (Alligator mississippiensis). Physiological and Biochemical Zoology 83 (4): 561-575 (cover). PDF

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