Chromosomal Replication, Translocation and Recombination as Putative Events in the Diversification of Vertebrate...

AQP8-type water channels are expressed superficially in the plasma membrane or intracellularly in the inner mitochondrial membrane, where they respectively function in osmohomeostasis or as peroxiporins to alleviate oxidative stress. To date only single-copy AQP8 or AQP16 genes are known in tetrapods and two binary gene clusters composed of aqp8aa-aqp8ab and aqp8ba-aqp8bb in teleost fishes. Here, using phylogenomic and synteny analyses, we revise this view and show that bony fish aqp8aa, -ab, -ba and -bb genes are non-canonical co-orthologs that independently arose at chromosomal breakpoints. Conversely, canonical orthologs of tetrapod AQP8 are now detected in all vertebrate classes except hagfishes. In cartilaginous fishes, intact aqp8 orthologs and linked pseudogenes exist in squalomorph sharks and only fractionated aqp8-like pseudogenes in galeomorph sharks. Some isolated aqp8-like exons are detected in batoid ray genomes, while no aqp8-type coding sequences are currently found in holocephalan genomes. In the actinopterygian (ray-finned fish) lineage, the canonical ortholog of tetrapod AQP8 is estimated to have undergone gene translocation in their common ancestor ~400 million years ago but was subsequently inactivated or lost in many descendant lineages. In close temporal proximity to this gene translocation event, the actinopterygian aqp8aa-aqp8ab binary gene cluster was generated in the original syntenic locus, potentially as a result of meiotic recombination. Our data support a model of total chromosomal replication for the generation of AQP16 genes and the teleost aqp8ba-aqp8bb gene cluster. We further uncover additional duplicates in Strepsirrhini primates that provide an eminent example of the stochastic nature of neofunctionalization. The present data thus suggest that that common ancestral genome duplications combined with lineage-level chromosomal translocation, recombination and replication events contributed to the diversification of vertebrate AQP8-type genes.