Which came first, the lung or the breath?

Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery an d the venous outflow enters the heart separately from systemic and portal b lood at the sinus venosus (Polypteriformes) or the atrium (lungfish). or is delivered to a separate left atrium (tetrapods). The swimbladder, on the o ther hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate in tercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechani sms remains open. On the whole, air ventilatory mechanisms in the actinopte rygian lineage are similar among different groups. including Polypteriforme s, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possibl e separate origin of air breathing in actinopterygian and 'sarcopterygian' lines is in conflict with the postulated much more ancient origin of verteb rate air-breathing organs. New studies on the isolated brainstem preparatio n of the gar (Lepisosleus osseus) show a pattern of efferent activity assoc iated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete l ack of evidence for AO in chondrichthyans, and the isolated position of pla coderms for which buoyancy organs of uncertain homology have been demonstra ted, it is likely that homologous pharyngeal AO arose in the ancestors of e arly bony fish, and was pre-dated by behavioral mechanisms for surface (wat er) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swim bladder, whereas the paired ventral parts evolved into lungs. (C) 2001 Else vier Science inc. All rights reserved.