An Amelogenin Herbivore Motif, a Compacted Enamel Protein Matrix and Prismatic Enamel in Uromastyx Demonstrate Convergent Evolution in an Agamid Masticatory Apparatus

The evolution of species is tightly linked to the generation of new molecular and structural features through variation and selection. Here we have performed a detailed analysis of the jaw apparatus of the spiny-tailed lizard Uromastyx maliensis. Our comparative anatomy study highlights a closed tooth row and a monophyodont set of teeth, indicative of an evolved dentition beyond lepidosaur standards. On a microscopic level, Uromastyx enamel was thicker than the enamel of other lepidosaurs, featuring bundles of elongated crystallites ordered into prisms. The Uromastyx amelogenin protein revealed a lengthy polyproline tripeptide repeat insert consisting of 10 tripeptide repeats and similar to the bovine amelogenin ruminant insert. On a protein level, Uromastyx amelogenin self-assembled into 20 nm subunits, half the size of the 40 nm subunits in Iguana and similar to the diameter of mammalian amelogenin protein subunit compartments. Formation of 20 nm subunit compartments has been previously shown to be essential for enamel prism growth. These data demonstrate that Uromastyx lizards feature an evolved dentition indicative of convergent evolution adapted to extreme arid conditions, as demonstrated by enamel crystallites and prisms, an elongated "herbivore" motif in the enamel amelogenin protein sequence and compacted enamel protein subunits facilitating elongated apatite crystal growth. In a broader evolutionary biology context, our results suggest that jaws and teeth may evolutionarily converge to surpass traditional Lepidosaur molecular and enamel microanatomy features to facilitate feeding specialization and survival.