The Evolution of Lung-Gill Bimodal Breathing and the Homology of Vertebrate Respiratory Pumps

Abstract

SYNOPSIS. A comparative analysis of actinopterygian and sarcopterygian aerial buccal pumps indicates that the primitive pattern of air transfer differs fundamentally between these two clades. Actinopterygian fishes ventilate their lungs with a four-stroke buccal pump: the buccal cavity expands and fills with expired air, compresses to expel expired air, expands again to take in fresh air, and then compresses again to pump fresh air into the lungs. Lungfishes, caudates, and anurans expand and compress the buccal cavity only once per expiratory-inspiratory cycle, and thus use a two-stroke pump. Both of these bidirectional, aerial buccal pumps evolved from unidirectional, aquatic buccal pumps. The two-stroke aerial pump and the primitive aquatic pump used for gill irrigation share slow movements and may both be triggered by the same central rhythm generator. These similarities suggest that the two-stroke buccal pump evolved from the gill irrigation pump. Similarly, the four-stroke pump shares rapid movement and afferent triggering with aquatic suction feeding and coughing, suggesting that the four-stroke pump may have evolved from a combination of two suction feeding or coughing movements. Thus the differences between the actinopterygian and sarcopterygian aerial buccal pumps may be due to their independent evolution from different aquatic buccal pumps, rather than due to divergence from a single aerial buccal pump.