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Different species of toothed whales (Odontoceti) exhibit a variety of tooth forms and enamel types. Some odontocetes have highly prismatic enamel with Hunter-Schreger bands, whereas enamel is vestigial or entirely lacking in other species. Different tooth forms and enamel types are associated with alternate feeding strategies that range from biting and grasping prey with teeth in most oceanic and river dolphins to the suction feeding of softer prey items without the use of teeth in many beaked whales. At the molecular level, previous studies have documented inactivating mutations in the enamel-specific genes of some odontocete species that lack complex enamel. At a broader scale, however, it is unclear whether enamel complexity across the full diversity of extant Odontoceti correlates with the relative strength of purifying selection on enamel-specific genes. Here, we employ sequence alignments for seven enamel-specific genes (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) in 62 odontocete species that are representative of all extant families. The sequences for 33 odontocete species were obtained from databases, and sequences for the remaining 29 species were newly generated for this study. We screened these alignments for inactivating mutations (e.g., frameshift indels) and provide a comprehensive catalog of these mutations in species with one or more inactivated enamel genes. Inactivating mutations are rare in Delphinidae (oceanic dolphins) and Platanistidae/Inioidea (river dolphins) that have higher enamel complexity scores. By contrast, mutations are much more numerous in clades such as Monodontidae (narwhal, beluga), Ziphiidae (beaked whales), Physeteroidea (sperm whales), and Phocoenidae (porpoises) that are characterized by simpler enamel or even enamelless teeth. Further, several higher-level taxa (e.g., Hyperoodon, Kogiidae, Monodontidae) possess shared inactivating mutations in one or more enamel genes, which suggests loss of function of these genes in the common ancestor of each clade. We also performed selection (dN/dS) analyses on a concatenation of these genes and used linear regression and Spearman’s rank-order correlation to test for correlations between enamel complexity and two different measures of selection intensity (# of inactivating mutations per million years, dN/dS values). Selection analyses revealed that relaxed purifying selection is especially prominent in physeteroids, monodontids, and phocoenids. Linear regressions and correlation analyses revealed a strong negative correlation between selective pressure (dN/dS values) and enamel complexity. Stronger purifying selection (low dN/dS) is found on branches with more complex enamel and weaker purifying selection (higher dN/dS) occurs on branches with less complex enamel or enamelless teeth. As odontocetes diversified into a variety of feeding modes, in particular, the suction capture of prey, a reduced reliance on the dentition for prey capture resulted in the relaxed selection of genes that are critical to enamel development.
Randall et al. (Sat,) studied this question.