Evolution of air-breathing and central CO(2)/H(+) respiratory chemosensitivity: new insights from an old fish?
While little is known of the origin of air-breathing in vertebrates, primitive air breathers can be found among extant lobe-finned (Sarcopterygii) and ray-finned (Actinopterygii) fish. The descendents of Sarcopterygii, the tetrapods, generate lung ventilation using a central pattern generator, the activity of which is modulated by central and peripheral CO(2)/H(+) chemoreception. Air-breathing in Actinopterygii, in contrast, has been considered a 'reflexive' behaviour with little evidence for central CO(2)/H(+) respiratory chemoreceptors. Here, we describe experiments using an in vitro brainstem preparation of a primitive air-breathing actinopterygian, the longnose gar Lepisosteus osseus. Our data suggest (i) that gill and air-breathing motor patterns can be produced autonomously by the isolated brainstem, and (ii) that the frequency of the air-breathing motor pattern is increased by hypercarbia. These results are the first evidence consistent with the presence of an air-breathing central pattern generator with central CO(2)/H(+) respiratory chemosensitivity in any primitive actinopterygian fish. We speculate that the origin of the central neuronal controller for air-breathing preceded the divergence of the sarcopterygian and actinopterygian lineages and dates back to a common air-breathing ancestor.
Wilson
R J
RJ
Department of Medical Physiology and Biophysics, Heritage Medical Research Building, University of Calgary, Calgary, Alberta, Canada T2N 4N1. wilsonr@acs.ucalgary.ca
Harris
M B
MB
Remmers
J E
JE
Perry
S F
SF
D000818:Animals; D005075:Biological Evolution; D001933:Brain Stem / Q000502:physiology; D002245:Carbon Dioxide; D002628:Chemoreceptor Cells; D005399:Fishes / Q000502:physiology*; D005880:Gills / Q000502:physiology; D006859:Hydrogen; D012119:Respiration
D002245:Carbon Dioxide; D006859:Hydrogen