Fitness consequences of genetic and phenotypic chimeras in the social amoeba, Dictyostelium discoideum

Multicellular organisms regularly eliminate unfit or harmful cells in the process of normal development. This high level of cooperation is maintained because all cells within the organism are genetically identical and thus, have the same evolutionary interests. However, there are some multicellular organisms that develop not from a single cell but from many individuals. In the case of the social amoebae, Dictyostelium discoideum, the usually solitary amoebae aggregate with nearby cells when starving to form a motile, multicellular slug that migrates to the soil surface and forms a fruiting body consisting of a bail of spores held aloft by a stalk of dead cells. These aggregations may be a mix of genetically identical individuals or of multiple clones, called genetic chimeras. Within chimeras, a conflict may arise over which cells contribute to the reproductive spores versus the dead stalk. Previous work on D. discoideum has shown that uniclonal slugs migrate further than chimeric slugs of the same size across agar. Here we test whether this resuits in a fitness cost under more natural conditions. We examined migration of slugs across decaying leaves and soil as well as migration up through layers of these substrates, closely reflecting the natural migration of D. discoideum slugs in the wild. In most trials, chimeras performed worse than single clones. Thus, chimerism in D. discoideum should produce a fitness cost likely to be important in nature. Since D. discoideum readily mixes with multiple clones, the potential for conflict is high. Diverging evolutionary interests in chimeras could influence adaptive strategies for filling the spore and stalk roles. Here we explore the strategy for filling these roles in phenotypic chimeras, mixes of cells differing only in physical condition. We explore the fitness of D. discoideum spores and found that cells with better prospects tend to represent the subsequent generations. However, we also found that D. discoideum amoebae did not respond to the condition of cells with which they aggregate. Our results indicate that, within a genetically identical population, the differentiation of spore and stalk roles is a competition based on the condition of the individual cells