Molecular evolution of neurohypophysial hormones in relation to osmoregulation: the two fish options

In vertebrates, water and osmolyte homeostasis is controlled by at least three hormonal systems: the hypothalamo-neurohypophysial system, the renin-angiotensin-aldosterone system and the atrial natriuretic factor system. The first system implies neuroendocrine reflexes involving an afferent neural limb from osmo- and baroreceptors to hypothalamus and an efferent endocrine limb from secretory neurons to target cell receptors and transduction to intracellular effectors, namely water and sodium channels. Evolution can affect any level of this molecular cascade. Whereas virtually all vertebrate species have two neurohypophysial hormones, an oxytocin-like and a vasopressin-like peptides, the most primitive vertebrates, Cyclostomata (lampreys and hagfishes) possess a single peptide, vasotocin, so that an early gene duplication occurred before the emergence of fishes, about 400 million years ago. The remarkable evolutionary stability of neurohypophysial hormones in bony vertebrates allows us to trace two main lineages: isotocin-mesotocin-oxytocin and vasotocin-vasopressin. In contrast, in cartilaginous fishes, the oxytocin-like peptides display a great evolutionary diversity: we have identified glumitocin in rays, aspargtocin and valitocin in the spiny dogfish, asvatocin and phasvatocin in the spotted dogfish, and oxytocin in the chimaera. Whereas bony vertebrates regulate their blood osmotic pressure (about 250–450 mOsm kg^-1 H₂O) essentially through salts, cartilaginous fishes use urea as the main osmolyte for adjusting their osmotic pressure above the external medium (about 1050 mOsm kg^-1 H₂O for marine fishes). The hypothesis is made that the stability of neurohypophysial hormones in bony vertebrates is due to their implication in ion-based osmoregulation (selective evolution), whereas in Chondrichthyes the occurrence of urea-based osmoregulation has relieved the hormones from this function and therefore made them free to vary (neutral evolution).