Convergent Evolution Has Led to the Loss of Claw Proteins in Snakes and Worm Lizards

The evolution of cornified skin appendages, such as hair, feathers, and claws, is closely linked to the evolution of proteins that establish the unique mechanical stability of these epithelial structures. We hypothesized that the evolution of the limbless body anatomy of the Florida worm lizard (Rhineura floridana) and the concomitant loss of claws had led to the degeneration of genes with claw-associated functions. To test this hypothesis, we investigated the evolution of three gene families implicated in epithelial cell architecture, namely type I keratins, type II keratins, and genes of the epidermal differentiation complex in R. floridana in comparison with other squamates. We report that the orthologs of mammalian hair and nail keratins have undergone pseudogenization in R. floridana. Likewise, the epidermal differentiation complex genes tentatively named EDYM1 and EDCCs have been lost in R. floridana. The aforementioned genes are conserved in various lizards with claws, but not in snakes. Proteomic analysis of the cornified claws of the bearded dragon (Pogona vitticeps) confirmed that type I and type II hair keratin homologs, EDYM1 and EDCCs, are protein components of claws in squamates. We conclude that the convergent evolution of a limbless body was associated with the convergent loss of claw keratins and differentiation genes in squamates.