Molecular Decay of the Tooth Gene Enamelin (ENAM) Mirrors the Loss of Enamel in the Fossil Record of Placental Mammals

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Abstract
Vestigial structures occur at both the anatomical and molecular levels, but studies documenting the co-occurrence of morphological degeneration in the fossil record and molecular decay in the genome are rare. Here, we use morphology, the fossil record, and phylogenetics to predict the occurrence of “molecular fossils” of the enamelin (ENAM) gene in four different orders of placental mammals (Tubulidentata, Pholidota, Cetacea, Xenarthra) with toothless and/or enamelless taxa. Our results support the “molecular fossil” hypothesis and demonstrate the occurrence of frameshift mutations and/or stop codons in all toothless and enamelless taxa. We then use a novel method based on selection intensity estimates for codons (ω) to calculate the timing of iterated enamel loss in the fossil record of aardvarks and pangolins, and further show that the molecular evolutionary history of ENAM predicts the occurrence of enamel in basal representatives of Xenarthra (sloths, anteaters, armadillos) even though frameshift mutations are ubiquitous in ENAM sequences of living xenarthrans. The molecular decay of ENAM parallels the morphological degeneration of enamel in the fossil record of placental mammals and provides manifest evidence for the predictive power of Darwin's theory. Enamel is the hardest substance in the vertebrate body. One of the key proteins involved in enamel formation is enamelin. Most placental mammals have teeth that are capped with enamel, but there are also lineages without teeth (anteaters, pangolins, baleen whales) or with enamelless teeth (armadillos, sloths, aardvarks, pygmy and dwarf sperm whales). All toothless and enamelless mammals are descended from ancestral forms that possessed teeth with enamel. Given this ancestry, we predicted that mammalian species without teeth or with teeth that lack enamel would have copies of the gene that codes for the enamelin protein, but that the enamelin gene in these species would contain mutations that render it a nonfunctional pseudogene. To test this hypothesis, we sequenced most of the protein-coding region of the enamelin gene in all groups of placental mammals that lack teeth or have enamelless teeth. In every case, we discovered mutations in the enamelin gene that disrupt the proper reading frame that codes for the enamelin protein. Our results link evolutionary change at the molecular level to morphological change in the fossil record and also provide evidence for the enormous predictive power of Charles Darwin's theory of descent with modification.