Evolution of BMP signaling in Drosophila oogenesis: a receptor-based mechanism

The bone morphogenetic protein (BMP) signaling pathway is a conserved regulator of cellular and developmental processes in animals. The mechanisms underlying BMP signaling activation differ among tissues and mostly reflect changes in the expression of pathway components. BMP signaling is one of the major pathways responsible for the patterning of the Drosophila eggshell, a complex structure derived from a layer of follicle cells (FCs) surrounding the developing oocyte. Activation of BMP signaling in the FCs is dynamic. Initially, signaling is along the anterior-posterior (A/P) axis; later, signaling acquires dorsal-ventral (D/V) polarity. These dynamics are regulated by changes in the expression pattern of the type I BMP receptor thickveins (tkv). We recently found that signaling dynamics and TKV patterning are highly correlated in the FCs of multiple Drosophila species. In addition, we showed that signaling patterns are spatially different among species. Here, we use a mathematical model to simulate the dynamics and differences of BMP signaling in numerous species. This model predicts that qualitative and quantitative changes in receptor expression can lead to differences in the spatial pattern of BMP signaling. We tested these predications experimentally in three different Drosophila species and through genetic perturbations of BMP signaling in D. melanogaster. On the basis of our results, we concluded that changes in tkv patterning can account for the experimentally observed differences in the patterns of BMP signaling in multiple Drosophila species.