The Provenance of Alveolar and Parabronchial Lungs: Insights from Paleoecology and the Discovery of Cardiogenic, Unidirectional Airflow in the American Alligator (Alligator mississippiensis)

Abstract

Birds and mammals evolved greater aerobic abilities than their common ancestor had. This required expansion of the cardiopulmonary system's capacity for gas exchange, but while directional selection for this expanded capacity resulted in extremely similar avian and mammalian hearts, strikingly different lungs arose, and the reasons for this divergence in lung morphology are not understood. In birds, gas exchange occurs in the lungs as air moves through small tubes (parabronchi) in one direction; in mammals, air flows tidally into and out of the alveoli. Here, I present a scenario for the origin of both the alveolar and parabronchial lungs that explains when and how they could have arisen by a gradual sequence of steps. I argue that (1) the alveolar lung evolved in the late Paleozoic, when high levels of atmospheric oxygen relaxed selection for a thin blood-gas barrier within the lung; (2) unidirectional flow originated in the ectothermic ancestral archosaur, the forerunner of birds and crocodilians, to enable the heart to circulate pulmonary gases during apnea. This hypothesis would be supported by a demonstration of unidirectional flow in the lungs of crocodilians, the extant sister taxon of birds. Airflow in the lungs of juvenile alligators was measured during apnea using dual thermistor flowmeters, and cardiac activity was measured with electrocardiography. Coincident with each heartbeat, a pulse of air flowed in the pulmonary conduit under study with a bias in the direction of movement, yielding a net unidirectional flow. These data suggest the internal structures requisite for unidirectional flow were present in the common ancestors of birds and crocodilians and may have preadapted the lungs of archosaurs to function advantageously during the oxygen-poor period of the early Mesozoic.