Historical reconstructions of evolving physiological complexity:O2 secretion in the eye and swimbladder of fishes

Abstract

SUMMARYThe ability of some fishes to inflate their compressible swimbladder with almost pure oxygen to maintain neutral buoyancy, even against the high hydrostatic pressure several thousand metres below the water surface, has fascinated physiologists for more than 200 years. This review shows how evolutionary reconstruction of the components of such a complex physiological system on a phylogenetic tree can generate new and important insights into the origin of complex phenotypes that are difficult to obtain with a purely mechanistic approach alone. Thus, it is shown that oxygen secretion first evolved in the eyes of fishes, presumably for improved oxygen supply to an avascular, metabolically active retina. Evolution of this system was facilitated by prior changes in the pH dependence of oxygen-binding characteristics of haemoglobin (the Root effect) and in the specific buffer value of haemoglobin. These changes predisposed teleost fishes for the later evolution of swimbladder oxygen secretion, which occurred at least four times independently and can be associated with increased auditory sensitivity and invasion of the deep sea in some groups. It is proposed that the increasing availability of molecular phylogenetic trees for evolutionary reconstructions may be as important for understanding physiological diversity in the postgenomic era as the increase of genomic sequence information in single model species.