Evolutionarily conserved waves of tooth replacement in the gecko are dependent on local signaling

Abstract

The fossil record contains dinosaur jaws with rows of unerupted successional teeth that are arranged in a variety of elegant patterns. The remnants of these patterns are visible in modern dentate reptiles but the mechanism for generating and maintaining these rows of teeth is unknown. The biology underlying the tooth replacement pattern was hypothesized to either be stimuli transmitted across tooth families in the jaws (Edmund) or secretion of local inhibitory molecules that would stagger development of adjacent tooth families (Osborn). To test these hypotheses and generate new ones, we completed a study on 6 treated adult geckos in which one side of the jaw had teeth removed. Wax bites were used to record the maxillary teeth 2 times a week. Tooth presence or absence was recorded and transformed mathematically. The time between eruption at each tooth position was measured as was the relative phase compared to the immediate adjacent teeth over successive bites. The period between eruption events at each tooth position was approximately 30 days with some lengthening over time. The average relative phase showed there was a tilt in the data that fit the observation that alternating teeth were being shed. This tilt was opposite on the left and right sides of the jaw. The asymmetry of the right and left sides was consistent across the dentition. After plucking, the pattern recovers after 3 periods fitting with the consistent finding that there are 3 teeth in each tooth family. Ablated areas did not recover tooth formation even after 14 months. The plucked animals showed evidence of fixed, local signaling that restores the pattern. Two models based on Osborn’s concept of a “zone of inhibition” deviate from the observed data. The ablated animals show no change in patterns of tooth eruption anterior and posterior to the gap. Thus there is no support for the Wave stimulus theory of Edmund. Finally, we propose a new Phase Inhibition Model. This model assumes fixed initiation sites at which teeth are initiated at some phase within a month-long cycle and that, as a tooth is initiated, the cycles of nearby initiation sites are inhibited in their progress. This inhibition causes nearest neighbours to erupt in anti-synchrony. This model best maintained the tilt, spacing timing of the real biological data. Mathematical modeling was sensitive enough to measure the normal developmental instability and the resilience of the gecko to restore homeostasis after tooth removal.