Pseudogenization of the tooth gene enamelysin (MMP20) in the common ancestor of extant baleen whales

Abstract

Whales in the suborder Mysticeti are filter feeders that use baleen to sift zooplankton and small fish from ocean waters. Adult mysticetes lack teeth, although tooth buds are present in foetal stages. Cladistic analyses suggest that functional teeth were lost in the common ancestor of crown-group Mysticeti. DNA sequences for the tooth-specific genes, ameloblastin (AMBN), enamelin (ENAM) and amelogenin (AMEL), have frameshift mutations and/or stop codons in this taxon, but none of these molecular cavities are shared by all extant mysticetes. Here, we provide the first evidence for pseudogenization of a tooth gene, enamelysin (MMP20), in the common ancestor of living baleen whales. Specifically, pseudogenization resulted from the insertion of a CHR-2 SINE retroposon in exon 2 of MMP20. Genomic and palaeontological data now provide congruent support for the loss of enamel-capped teeth on the common ancestral branch of crown-group mysticetes. The new data for MMP20 also document a polymorphic stop codon in exon 2 of the pygmy sperm whale (Kogia breviceps), which has enamel-less teeth. These results, in conjunction with the evidence for pseudogenization of MMP20 in Hoffmann's two-toed sloth (Choloepus hoffmanni), another enamel-less species, support the hypothesis that the only unique, non-overlapping function of the MMP20 gene is in enamel formation.

Evidence for a single loss of mineralized teeth in the common avian ancestor

“…The inactivation of enamel-related genes parallels the loss of enamel in the mammalian fossil record (4,(11)(12)(13). The presence of shared, inactivating mutations in dentin-and enamel-related genes could therefore be used as a molecular proxy to assess whether teeth were lost once or on multiple occasions in the common ancestor of living birds, as well as to estimate the timing of tooth loss.…”

“…Of the hundreds of genes associated with tooth development, most are pleiotropic and perform essential functions outside of tooth development (15). By contrast, the aforementioned six genes have been hypothesized to be tooth-specific based on mutagenesis studies in mice, inactivation of these genes in one or more edentulous/enamelless vertebrate species, and natural genetic variation in humans that causes nonsyndromic amelogenesis imperfecta, dentinogenesis imperfecta, and dentin dysplasia (11)(12)(13)(16)(17)(18)(19)(20) (table S1). At the same time, other evidence indicates that these six genes are pleiotropic and are expressed outside of tooth development (21)(22)(23) (table S1).…”

“…Convergent enamel loss within Xenarthra is inferred for Pilosa (sloths and anteaters) and multiple armadillo lineages (4). Information on the enam-and dentin-related genes for pygmy/dwarf sperm whales, anteaters, and baleen whales are from previous studies (4,11,12,16,44). Hypothesized loss of mineralized teeth on the stem neornithine branch is assumed on the basis of indel substitution rates (27,43).…”

“…In each case, closely related extinct (Odontochelys, Ichthyornis, Eomaia, and Aetiocetus) and extant dentate taxa are also shown. Estimates for the timing of enamel loss in mammals are from fossils, phylogenetics, molecular clocks, frameshift mutations, and/or ratio of nonsynonymous to synonymous substitutions (dN/dS) (4,12). Convergent enamel loss within Xenarthra is inferred for Pilosa (sloths and anteaters) and multiple armadillo lineages (4).…”

Decoupling Tooth Loss from the Evolution of Baleen in Whales

“…The presence of rudimentary teeth in extant mysticete fetuses (Saint-Hilaire, 1807;Karlsen, 1962) reflects this ancestry, but the developmental mechanisms responsible for tooth loss in utero remain obscure. Molecular data suggests that a single transformation to toothless adults occurred in the common ancestor of all living mysticetes (Meredith et al, 2011). This argument is broadly supported by new fossil discoveries of stem Mysticeti, although the increasing diversity of toothed and toothless states in new stem taxa points to a more complex transition from raptorial feeding to filter feeding than suggested by step-wise models .…”