Chemolithoautotrophic, sulphide-oxidizing (thiotrophic) symbioses represent spectacular adaptations to fluctuating environmental gradients and survival is often accomplished when growth is fuelled by sufficient nourishment through the symbionts leading to fast cell proliferation. Here we show 5′-bromo-2′ deoxyuridine (BrdU) pulse labelling of vegetative growingZoothamnium niveum, a colonial ciliate obligately associated with thiotrophic ectosymbionts, and demonstrate age related growth profiles in three heteromorphic host cell types. At the colony’s apex, a large top terminal zooid performed high proliferation activity, which decreased significantly with increasing colony age but was still present in old colonies indicating that this cell possesses lifelong cell division potential. In contrast, terminal branch zooids proliferated independent of colony age but appeared to be limited by their cell division capacity predetermined by branch size, thus leading to the strict, feather-shaped colony form. Appearance of labelled terminal branch zooids allowed us to distinguish a highly proliferating apical colony region from an almost inactive, senescent basal region. In macrozooids attached to the colony, extensive BrdU labelling suggests that DNA synthesis occurs in preparation for a new generation. As motile swarmers, the macrozooids seem to be arrested in the cell cycle and mitosis and cell division occur when the swarmer settles and transforms into a top terminal zooid buildingup a new colony.