Evolution of different life-cycle strategies in oceanic calcareous dinoflagellates

The formation of non-motile resting cysts within the dinoflagellate life-cycle has long been considered to be unsuitable for open oceanic environments, because a considerable part of a population might be lost due to sinking. An alternative life-cycle with the production of vegetative calcareous cells as the dominant life-cycle stage was reported for the oceanic calcareous dinoflagellate Thoracosphaera heimii, and earlier observations suggested that other oceanic calcareous dinoflagellates might have similar life-cycles. In order to test this hypothesis, we investigated the life-cycle of three oceanic calcareous dinoflagellates, Thoracosphaera heimii, Leonella granifera and Calciodinellum levantinum in culture and determined relative ploidy levels with confocal laser scanning microscopy. Whereas C. levantinum forms calcareous resting cysts within the diploid sexual life-cycle phase, T. heimii and L. granifera form vegetative calcareous cells within the haploid asexual phase. By comparison with recently published molecular phylogenies, we conclude that C. levantinum is part of a group of mainly neritic species, from which oceanic species evolved repeatedly. The life-cycle of C. levantinum is basically identical to that of its neritic relatives. A reduced dormancy period is interpreted as an adaptation to the oceanic environment. By contrast, T. heimii and L. granifera are part of a clade of dinoflagellates in which the haploid vegetative life- cycle phase has diversified and enabled their members to access new habitats. While the primary calcification during the diploid phase was lost in this group, calcification was regained secondarily in the haploid vegetative life- cycle phase in T. heimii and L. granifera. Therefore the vegetative calcareous cells are not homologous with the calcareous resting cysts formed in other calcareous dinoflagellates, which may also be expressed in different biomineralization modes.