Independent origins of spicules reconcile palaeontological and molecular evidence of sponge evolutionary history

Sponges (Porifera) play a critical role in global biogeochemical processes. However, their evolutionary timeline remains unclear hampering our understanding of Neoproterozoic paleoecology. Molecular data suggest a Tonian or Cryogenian origin, while the oldest confirmed sponge fossils, represented by siliceous spicules, date to the Ediacaran. To understand this 150-million-year discrepancy, we compiled a new phylogenomic dataset, revised fossil evidence, derived a new dated sponge phylogeny, and tested whether ancestral sponges were aspiculated or not. We infer the last common sponge ancestor to have been early Ediacaran in age and aspiculated. Siliceous spicules evolved independently at least four times, and calcareous spicules at least two times in crown sponges. We performed a diversification rate analysis showing that siliceous spicules did not drive species radiations. Our study reconciles molecular and fossil evidence, indicating that while sponges emerged in the early Ediacaran, they are largely absent from the Neoproterozoic fossil record because they had not yet evolved spicules. TeaserSponges emerged in the Precambrian, were soft-bodied and did not produce mineralized spicules, which emerged multiple times independently.