Developmental system drift in dorsoventral patterning is linked to transitions to autonomous development in Annelida

Abstract The Bone Morphogenetic Protein (BMP) pathway is the ancestral signalling system patterning the dorsoventral axis in bilaterally symmetrical animals. However, in Spiralia, a large bilaterian clade including molluscs and annelids, BMP’s axial function varies across species, obscuring the ancestral developmental role of this pathway. Here, we study four annelid species to demonstrate that BMP is ancestrally downstream of ERK1/2 and promotes dorsoventral development in Annelida. Importantly, this signalling hierarchy is lost in annelids that secondarily transitioned to a maternally controlled, unequal cleavage, with some using Activin/Nodal and others relying on BMP to establish dorsoventral polarity only in the head. Unexpectedly, this divergence implies extensive rewiring of downstream targets involved in dorsoventral patterning. Together, our data clarify BMP’s ancestral axial role in Spiralia, uncovering a potential causal link between parallel shifts toward unequal spiral cleavage and the emergence of developmental system drift, a pervasive yet poorly understood phenomenon in animal embryogenesis.