Abstract
The birth of novel genes, including their cell-specific transcriptional control, is a major source of evolutionary innovation. The lens-preferred proteins, crystallins (vertebrates: α- and β/γ-crystallins), provide a gateway to study eye evolution. Diversity of crystallins was thought to originate from convergent evolution through multiple, independent formation of Pax6/PaxB-binding sites within the promoters of genes able to act as crystallins. Here, we propose that αB-crystallin arose from a duplication of small heat shock protein (Hspb1-like) gene accompanied by Pax6-site and heat shock element (HSE) formation, followed by another duplication to generate the αA-crystallin gene in which HSE was converted into another Pax6-binding site. The founding β/γ-crystallin gene arose from the ancestral Hspb1-like gene promoter inserted into a Ca2+-binding protein coding region, early in the cephalochordate/tunicate lineage. Likewise, an ancestral aldehyde dehydrogenase (Aldh) gene, through multiple gene duplications, expanded into a multigene family, with specific genes expressed in invertebrate lenses (Ω-crystallin/Aldh1a9) and both vertebrate lenses (η-crystallin/Aldh1a7 and Aldh3a1) and corneas (Aldh3a1). Collectively, the present data reconstruct the evolution of diverse crystallin gene families.