BackgroundThe gene for odontogenic ameloblast-associated (ODAM) is a member of the secretory calcium-binding phosphoprotein gene family. ODAM is primarily expressed in dental tissues including the enamel organ and the junctional epithelium, and may also have pleiotropic functions that are unrelated to teeth. Here, we leverage the power of natural selection to test competing hypotheses that ODAM is tooth-specific versus pleiotropic. Specifically, we compiled and screened complete protein-coding sequences, plus sequences for flanking intronic regions, for ODAM in 165 placental mammals to determine if this gene contains inactivating mutations in lineages that either lack teeth (baleen whales, pangolins, anteaters) or lack enamel on their teeth (aardvarks, sloths, armadillos), as would be expected if the only essential functions of ODAM are related to tooth development and the adhesion of the gingival junctional epithelium to the enamel tooth surface.ResultsWe discovered inactivating mutations in all species of placental mammals that either lack teeth or lack enamel on their teeth. A surprising result is that ODAM is also inactivated in a few additional lineages including all toothed whales that were examined. We hypothesize that ODAM inactivation is related to the simplified outer enamel surface of toothed whales. An alternate hypothesis is that ODAM inactivation in toothed whales may be related to altered antimicrobial functions of the junctional epithelium in aquatic habitats. Selection analyses on ODAM sequences revealed that the composite dN/dS value for pseudogenic branches is close to 1.0 as expected for a neutrally evolving pseudogene. DN/dS values on transitional branches were used to estimate ODAM inactivation times. In the case of pangolins, ODAM was inactivated ~ 65 million years ago, which is older than the oldest pangolin fossil (Eomanis, 47 Ma) and suggests an even more ancient loss or simplification of teeth in this lineage.ConclusionOur results validate the hypothesis that the only essential functions of ODAM that are maintained by natural selection are related to tooth development and/or the maintenance of a healthy junctional epithelium that attaches to the enamel surface of teeth.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1359-6) contains supplementary material, which is available to authorized users.

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The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a 'transitional chimaeric feeder' scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of 'dental genes' related to enamel formation before the emergence of crown Mysticeti, while 'baleen genes' that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.

The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.

The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a transitional chimaeric feeder scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of dental genes related to enamel formation before the emergence of crown Mysticeti, while baleen genes that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.