Convergent evolution of type I antifreeze proteins from four different progenitors in response to global cooling

The alanine-rich, alpha-helical type I antifreeze proteins (AFPs) in fishes are thought to have arisen independently in the last 30 ma on at least four occasions. This hypothesis has recently been proven for the flounder and sculpin AFPs that both originated by gene duplication and divergence followed by substantial gene copy number expansion. Here we have examined the origins of the cunner (wrasse) and snailfish (liparid) AFPs. The cunner AFP has arisen by a similar route from the duplication and divergence of a GIMAP gene. The coding region for this AFP stems from an alanine-rich region flanking the GTPase domain of GIMAPa. The AFP gene has remained in the GIMAP gene locus and undergone amplification there along with some GIMAPa genes. The AFP gene originated after the cunner diverged from the common ancestor to the closely related spotty and ballan wrasses that have a similar gene synteny but are completely lacking the AFP genes. Snailfish AFPs have also recently evolved because they are confined to a single genus of this family. In these AFP-producing species the AFP locus does not share any similarity to functional genes. Instead, it is replete with repetitive DNAs and transposons several stretches of which could code for tracts of alanine with a dominant codon (GCC) that matches the bias seen in the AFP genes. All four known instances of type I AFPs occurring in fishes are independent evolutionary events that happened soon after the onset of northern hemisphere Cenozoic glaciation events. Collectively they provide a remarkable example of convergent evolution to one AFP type.