Compatible and counteracting solutes and the evolution of ion and osmoregulation in fishes

Abstract

The evolution of ion and osmoregulation in fishes can be divided into three physiological stages. The first stage is a strategy employed by extant hagfish and involved a reduction of inorganic ion levels intracellularly through the use of compatible organic solutes. During osmotic stress, the concentration of organic solutes changes to aid in cell volume regulation, but both intracellular and plasma inorganic ion levels may fluctuate. The next step involved substitution of a permeable and rapidly diffusing, nonmetabolizable organic solute (urea) for some of the other compatible organic solutes. This strategy is utilized by extant chondrichthians and the coelacanth. Specific levels of methylamines are maintained in the cells and extracellular fluids of these organisms to counteract adverse physicochemical effects of urea. Species using this strategy possess greater control of intracellular ion levels during osmotic stress. Reduced and relatively constant intracellular concentrations of inorganic ions minimize disruptive effects of osmotic stress on cell and mitochondrial membrane potentials. The final step in the evolution of control of the intracellular milieu during osmotic stress is the most energetically expensive. In actinopterygians, extracellular inorganic ion levels are controlled by special tissues (kidneys and gills) that also maintain tissue osmolarity relatively constant in environments of variable osmolarity. It is suggested that atmospheric oxygen levels at various times during the evolution of the fishes had a role in determining the osmotic strategy employed by different groups of fishes.