Mammalian molar complexity follows simple, predictable patterns

Identifying developmental explanations for the evolution of complex structures like mammalian molars is fundamental to studying phenotypic variation. Previous study showed that a “morphogenetic gradient” of molar proportions was explained by a balance between inhibiting/activating activity from earlier developing molars, termed the inhibitory cascade model (ICM). Although this model provides an explanation for variation in molar proportions, what remains poorly understood is if molar shape, or specifically complexity (i.e., the number of cusps, crests), can be explained by the same developmental model. Here, we show that molar complexity conforms to the ICM, following a linear, morphogenetic gradient along the molar row. Moreover, differing levels of inhibiting/activating activity produce contrasting patterns of molar complexity depending on diet. This study corroborates a model for the evolution of molar complexity that is developmentally simple, where only small-scale developmental changes need to occur to produce change across the entire molar row, with this process being mediated by an animal’s ecology. The ICM therefore provides a developmental framework for explaining variation in molar complexity and a means for testing developmental hypotheses in the broader context of mammalian evolution.

Functional evolution of a morphogenetic gradient

Bone Morphogenetic Proteins (BMPs) pattern the dorsal-ventral axis of bilaterian embryos; however, their roles in the evolution of body plan are largely unknown. We examined their functional evolution in fly embryos. BMP signaling specifies two extraembryonic tissues, the serosa and amnion, in basal-branching flies such as Megaselia abdita, but only one, the amnioserosa, in Drosophila melanogaster. The BMP signaling dynamics are similar in both species until the beginning of gastrulation, when BMP signaling broadens and intensifies at the edge of the germ rudiment in Megaselia, while remaining static in Drosophila. Here we show that the differences in gradient dynamics and tissue specification result from evolutionary changes in the gene regulatory network that controls the activity of a positive feedback circuit on BMP signaling, involving the tumor necrosis factor alpha homolog eiger. These data illustrate an evolutionary mechanism by which spatiotemporal changes in morphogen gradients can guide tissue complexity.