Comparative physiology of the pulmonary circulation.

Two selective pressures have shaped the evolution of the pulmonary circulation. First, as animals evolved from heterothermic ectotherms to homeothermic endoderms with their corresponding increase in the ability to sustain high oxygen consumptions, the blood-gas barrier had to become successively thinner, and also provide an increasingly large area for diffusive gas exchange. Second, the barrier had to find a way to maintain its mechanical integrity in the face of extreme thinness, and this was assisted by the increasing separation of the pulmonary from the systemic circulation. A remarkable feature throughout the evolution of air-breathing vertebrates has been the tight conservation of the tripartite structure of the blood-gas barrier with its three layers: capillary endothelium, extracellular matrix, and alveolar epithelium. The strength of the barrier can be ascribed to the very thin layer of type IV collagen in the extracellular matrix. In the phylogenic progression from amphibia and reptiles to mammals and birds, the blood-gas barrier became successively thinner. Also, the area increased greatly reflecting the greater oxygen demands of the organism. The gradual separation of the pulmonary from the systemic circulation continued from amphibia through reptiles to mammals and birds. Only in the last two classes are the circulations completely separate with the result that the pulmonary capillary pressures can be maintained low enough to avoid stress failure of the blood-gas barrier. Remarkably, the barrier is generally much thinner in birds than mammals, and it is also much more uniform in thickness. These advantages for gas exchange can be explained by the support of avian pulmonary capillaries by the surrounding air capillaries. This arrangement was made possible by the adoption of the flow-through system of ventilation in birds as opposed to the reciprocating pattern in mammals.