Single-cell phenotypic plasticity modulates social behaviour in Dictyostelium discoideum.

In Dictyostelium chimeras, strains social behaviour is defined based on their relative representation in the spores - the reproductive cells resulting from development - referred to as spore bias. Some strains, called cheaters, display systematically positive spore bias in chimeras and are considered a threat to the evolutionary stability of multicellular organization. The selective advantage gained by cheaters is indeed predicted to undermine collective functions whenever social behaviours are genetically determined. 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. Spore bias is shown to depend both on growth phase and on population composition, and to be negatively correlated to the fraction of loners, i.e. cells that do not join aggregates. We examined several single-cell mechanical properties that are expected to affect aggregation efficiency, and found that variations in the fraction of slowly moving cells with growth phase may explain why earlier cultures appear to be underrepresented in the spores. The involvement of a go-or-grow mechanism during cell aggregation is also consistent with known variations of cell-cycle phase distribution during population growth. We confirm the expected ubiquity of growth-phase induced spore bias variation by showing that it is not negligible in genetic chimeras, and can even reverse the classification of a strains social behaviour. These results suggest that aggregation can provide an efficient lottery system to harness the evolutionary spread of cheaters.