Single-cell phenotypic plasticity modulates social behaviour inDictyostelium discoideum

Abstract

In Dictyostelium chimeric aggregates, strains social behaviour is defined based on their relative representation in the spores, the reproductive cells resulting from development. Some strains, called "cheaters", that produce more than their fair share of spores are considered a threat to the evolutionary stability of multicellular organization. The selective advantage gained by cheaters is indeed predicted to lead to the progressive loss of collective functions whenever social behaviours are genetically determined and in the absence of mechanisms guaranteeing strong assortment. However, genotypes are not the only determinant of spore bias, and the relative role of genetic and plastic phenotypic differences in strains evolutionary success is unclear. Here, we control phenotypic heterogeneity by harvesting cells in different growth phases, and study the effects of plastic variation on spore bias in chimeras composed of isogenic or genetically different populations. Our results indicate that variation in cell mechanical properties induced by differences in populations growth phase affects their probability to aggregate, hence their chance to differentiate into spores during multicellular development. The contribution of this non-genetic source of variation to spore bias is non-negligible, and sometimes even overrides genetic differences between co-aggregating strains. These results support the idea that unavoidable variation in the timing of aggregation, a parameter that is not under the control of any single cell or genotype, can compete with selection on genetically determined traits. Our observations suggest that heterogeneity in mechanical properties during aggregation may contribute to limit the spread of "cheaters", thus to the evolutionary stability of aggregative multicellularity.