The case of homologous monomeric gamma-type and oligomeric beta-type crystallins has been described and analyzed in evolutionary terms. Data and hypotheses from molecular genetics and structural investigations converge and suggest a novel three-phase model for the evolutionary history of crystallin-type proteins. In the divergent cascades of monomeric and oligomeric crystallins, a pivotal role was played by alterations in the gene segments encoding the C-terminal extensions and the intermotif or interdomain linker peptides. These were genomic hot spots where evolution experimented to produce the modern variety of betagamma-crystallin-type quaternary structures.