Calcareous sponges develop in an unusual way. The embryo forms with internally facing cilia and turns inside out to produce the amphiblastula larva, with locomotory cilia directed outwards. The larva invaginates at metamorphosis, in a gastrulation-like manner, to form the juvenile sponge. Why these events happen has fascinated biologists for over a Century without resolution. We have been able to trace the movements of cytoplasmic determinants that mark the essential larval photoreceptor determinants through development. These shift from the oocyte to four blastomeres and then into four presumptive photoreceptor cells – the cross cells – in the larva whose positioning is critical to the behaviour and successful metamorphosis of the juvenile sponge. A metanalysis of genes expressed during the development of the genus Sycon shows while a range of genes do mark the cross cells once they have differentiated, few genes solely mark the oocyte and are carried through to the cross cells. Of those members of the Wnt pathway stand out as also having a highly polarized expression in both larva and adult. Our findings suggest that these cytoplasmic regions are markers of polarity that is maintained from oocyte through to the juvenile sponge by way of the type of cleavage divisions, and also by inversion of the embryo and invagination of the larva at metamorphosis. We consider whether the retention/preservation of polarity and precise positioning of cytoplasmic determinants during development of these sponges may be the equivalent of forming “germ layers” in other metazoans.