Yolk protein hydrolysis and oocyte free amino acids as key features in the adaptive evolution of teleost fishes to seawater

The ancestors of teleost fishes lived in freshwater for about 250 million years before returning to the sea during the Jurassic period. The hyposmotic blood of extant marine teleosts is assumed to reflect this freshwater origin. About 100 million years ago the palaeontological record shows a sudden differentiation of the teleosts with a burst of new species evolving. This transition from freshwater to the sea demanded certain osmotic adaptations in order to maintain homeostasis. These osmotic adaptations especially apply to the embryos since they lack the organs responsible for osmoregulation in the adult fish. At spawning, marine fish eggs must contain a water reservoir to compensate for the passive water loss imposed by the hyperosmotic seawater. The high water content of the yolk of marine teleost eggs reflects this water reservoir. Most extant marine fishes, regardless of systematic affinities, spawn pelagic eggs. A mechanism must have been established during teleost evolution to bring the water into the yolk before the eggs were spawned. Yolk protein hydrolysis and increase in content of free amino acids (FAA) during final oocyte maturation is part of this mechanism in extant marine teleosts with pelagic eggs. The oocyte FAA pool is generated mainly by hydrolysis of a similar to 100 kD yolk protein. This provides the osmotic drive for the water uptake into the oocyte. Intriguingly, this pool of FAA in pelagic teleost eggs is remarkably similar regardless of the taxonomic position of the species, implying that the hydrolysed fraction of the yolk protein is evolutionary conserved. This yolk protein is a fragment of the N-terminal end of a derivative of vitellogenin. In the authors' opinion, the establishment of the yolk protein hydrolysis at final oocyte maturation with the resulting increase in the FAA pool and oocyte hydration was a key step in teleost evolution that gave rise to their successful differentiation in the oceans about 100 million years ago.