Caste differentiation leading to reproductive division of labor is the hallmark of insect societies. Insect colonies typically contain mated queens that reproduce and workers with reduced fertility that undertake the tasks required for colony maintenance and development. Despite the prediction that the proportion of morphological castes should vary to enhance the fitness of colony members in response to environmental conditions, shifts in caste ratios have so far only been reported in a competitive situation. Societies of the ant Cerapachys biroi have evolved in an extraordinary way, in that queens and all workers reproduce through obligatory thelytokous parthenogenesis. Because workers of C. biroi represent the main reproductive force of the colony, the presence of such unmated queens seems puzzling. Here, we show that societies of C. biroi alter caste ratios by considerably increasing the production of queens when larvae are reared by sterile individuals in 2 situations: when senescent colonies are faced with food shortage or when well-fed larvae are reared by callow workers due to persisting plentiful resources. In the absence of these opposite conditions, larvae mostly develop into workers. Additional experiments suggest that these results are consistent with a contact pheromone to which larvae could be exposed when cared for by fertile individuals. In this species in which reproduction mainly relies on young workers with finite fertility, a self-regulated mechanism of caste differentiation could allow the enhancement of colony growth through worker production in fertile conditions or the restoration of colonial fertility through queen production in senescent societies. Copyright 2011, Oxford University Press.