Background Vertebrate teeth exhibit a wide range of regenerative systems. Many species, including most mammals, reptiles, and amphibians, form replacement teeth at a histologically distinct location called the successional dental lamina, while other species do not employ such a system. Notably, a ‘lamina-less’ tooth replacement condition is found in a paraphyletic array of ray-finned fishes, such as stickleback, trout, cod, medaka, and bichir. Furthermore, the position, renewal potential, and latency times appear to vary drastically across different vertebrate tooth regeneration systems. The progenitor cells underlying tooth regeneration thus present highly divergent arrangements and potentials. Given the spectrum of regeneration systems present in vertebrates, it is unclear if morphologically divergent tooth regeneration systems deploy an overlapping battery of genes in their naïve dental tissues. Results In the present work, we aimed to determine whether or not tooth progenitor epithelia could be composed of a conserved cell type between vertebrate dentitions with divergent regeneration systems. To address this question, we compared the pharyngeal tooth regeneration processes in two ray-finned fishes: zebrafish (Danio rerio) and threespine stickleback (Gasterosteus aculeatus). These two teleost species diverged approximately 250 million years ago and demonstrate some stark differences in dental morphology and regeneration. Here, we find that the naïve successional dental lamina in zebrafish expresses a battery of nine genes (bmpr1aa, bmp6, cd34, gli1, igfbp5a, lgr4, lgr6, nfatc1, and pitx2), while active Wnt signaling and Lef1 expression occur during early morphogenesis stages of tooth development. We also find that, despite the absence of a histologically distinct successional dental lamina in stickleback tooth fields, the same battery of nine genes (Bmpr1a, Bmp6, CD34, Gli1, Igfbp5a, Lgr4, Lgr6, Nfatc1, and Pitx2) are expressed in the basalmost endodermal cell layer, which is the region most closely associated with replacement tooth germs. Like zebrafish, stickleback replacement tooth germs additionally express Lef1 and exhibit active Wnt signaling. Thus, two fish systems that either have an organized successional dental lamina (zebrafish) or lack a morphologically distinct successional dental lamina (sticklebacks) deploy similar genetic programs during tooth regeneration. Conclusions We propose that the expression domains described here delineate a highly conserved “successional dental epithelium” (SDE). Furthermore, a set of orthologous genes is known to mark hair follicle epithelial stem cells in mice, suggesting that regenerative systems in other epithelial appendages may utilize a related epithelial progenitor cell type, despite the highly derived nature of the resulting functional organs.

Cleaning, a dietary strategy in which mucus or ectoparasites are removed and consumed off other taxa, is performed facultatively or obligately in a variety of species. We explored whether species in the Labridae (wrasses, parrotfishes) of varying ecological specialization employ similar mechanisms of prey capture. In investigating feeding on attached prey among juveniles of 19 species of wrasses, we found that patterns of biting in wrasses are influenced by the interaction between the maxilla and a feature of the premaxilla which we term the maxillary crest. Premaxillary motion during biting appears to be guided by the relative size of the crest. In many cases, this results in a 'premaxillary bite' wherein the premaxillae rapidly move anteroventrally to meet the lower jaws and deliver a protruded bite. Cleaners in the Labrichthyini tribe, however, exhibited reduced or absent maxillary crests. This coincided with a distinct kinematic pattern of prey capture in these labrichthyine cleaners, coupled with some of the fastest and lowest-excursion jaw movements. Although evidence of kinematic specialization can be found in these labrichthyines (most notably in the obligate cleaners in ), we found that facultative cleaners from other lineages similarly evolved reductions in excursions and timing. Convergence in feeding kinematics is thus apparent despite varying degrees of cleaning specialization and underlying morphological features.

BackgroundVertebrate teeth exhibit a wide range of regenerative systems. Many species, including most mammals, reptiles, and amphibians, form replacement teeth at a histologically distinct location called the successional dental lamina, while other species do not employ such a system. Notably, a ‘lamina-less’ tooth replacement condition is found in a paraphyletic array of ray-finned fishes, such as stickleback, trout, cod, medaka, and bichir. Furthermore, the position, renewal potential, and latency times appear to vary drastically across different vertebrate tooth regeneration systems. The progenitor cells underlying tooth regeneration thus present highly divergent arrangements and potentials. Given the spectrum of regeneration systems present in vertebrates, it is unclear if morphologically divergent tooth regeneration systems deploy an overlapping battery of genes in their naïve dental tissues.ResultsIn the present work, we aimed to determine whether or not tooth progenitor epithelia could be composed of a conserved cell type between vertebrate dentitions with divergent regeneration systems. To address this question, we compared the tooth regeneration processes in two ray-finned fishes: zebrafish (Danio rerio) and threespine stickleback (Gasterosteus aculeatus). These two teleost species diverged approximately 250 million years ago, and demonstrate some stark differences in dental morphology and regeneration. Here we find that the successional dental lamina in zebrafish sharply upregulates Wnt signaling and Lef1 expression during early morphogenesis stages of tooth development. Additionally, the naïve zebrafish successional dental lamina expresses a battery of nine genes (Bmpr1a, Bmp6, CD34, Gli1, Igfbp5a, Lgr4, Lgr6, Nfatc1, and Pitx2). We also find that, despite the absence of a histologically distinct successional dental lamina in stickleback tooth fields, new tooth germs also sharply upregulate Wnt signaling and Lef1 expression, and additionally express the same battery of nine genes in the basalmost endodermal cell layer from which replacement tooth epithelia arise. Thus, two fish systems that either have an organized successional dental lamina (zebrafish) or lack a morphologically distinct successional dental lamina (sticklebacks) deploy similar genetic programs during tooth regeneration.ConclusionsWe propose that the expression domains described here delineate a highly conserved “successional dental epithelium” (SDE). Furthermore, a set of orthologous genes is known to mark hair follicle epithelial stem cells in mice, suggesting that regenerative systems in other epithelial appendages may utilize a related epithelial progenitor cell type, despite the highly derived nature of the resulting functional organs.

Most vertebrates are capable of regenerating entire tooth organs. Tooth regeneration has long been hypothesized to rely on extracellular signals that can influence multiple tooth sites at once. Little is known about which secreted signaling molecules can influence this process. As an entry point, we asked whether fish orthologs of genes known to regulate mammalian hair regeneration have effects on tooth regeneration or total tooth number. We tested whether tooth regeneration could be accelerated by exogenous Wnt signaling (via Wnt10a) or BMP inhibition (Grem2a), and if regeneration rates were slowed by exogenous BMP signaling (Bmp6) or Wnt inhibition (Dkk2). Using two fish species that demonstrate distinct modes of whole tooth regeneration, the threespine stickleback (Gasterosteus aculeatus) and zebrafish (Danio rerio), we found that transgenic overexpression of four different genes changed tooth replacement rates in the predicted direction: Wnt10a and Grem2a increased the tooth replacement rate, while Bmp6 and Dkk2 strongly inhibited replacement tooth formation. Regulation of total tooth number was separable from regulation of regeneration rates. In zebrafish, none of the factors affecting regeneration rate affected the number of distinct tooth families but did sometimes affect total tooth number. In sticklebacks, which do not exhibit clear tooth families, Bmp6 and Dkk2 reduced total tooth number, while Wnt10a and Grem2a did not. These data support a model where different epithelial organs like teeth and hair share genetic inputs driving the timing of whole organ regenerative cycles.