Evolving social behaviour through selection of single-cell adhesion in Dictyostelium discoideum

Abstract

The social amoeba Dictyostelium discoideum commonly forms chimeric fruiting bodies by aggregation of different strains. Genetic variants that produce a higher proportion of spores are predicted to undercut multicellular organization unless cooperators assort positively. Cell adhesion is considered a primary factor driving such assortment, but evolution of adhesion has not been experimentally connected to changes in social performance. In this study we modified by experimental evolution the properties of individual cells, selecting for higher and lower adhesion to substrate. We then quantified the effects of these changes on cell-cell adhesion, development, and social behaviour. Unlike strains selected based on relative reproductive success in the social stage, we found that in binary chimeras both derived strains produce a smaller fraction of spores than the ancestor. Thus, evolution appears to have produced social cooperators. Examination of development revealed that this is however achieved via two opposed paths. Cells selected to be more adhesive to the substrate disproportionately contribute to the structural stability of fruiting bodies, as one would expect for cooperators. On the contrary, less adhesive cells behave as cheaters that undermine their own success more than that of the ancestor. These differences are reflected by a metric for social success that generalizes the classically used variation in frequency during the multicellular phase. Our work shows that cell mechanical interactions can constrain evolution of development and assortment in chimeras, and calls for integrating cell-level processes in conceptualizing the emergence of multicellular organization. Author summary The multicellular life cycle of Dictyostelium discoideum is as amazing as puzzling. Genetically different cells commonly co-aggregate, so that collective functions – that repose on cooperation among cells – are constantly threatened by the presence of exploitative variants, commonly called ‘cheaters’. Most previous studies focused on how reproductive success in the multicellular phase of the life cycle can be compensated by positive assortment of cooperating cells, but recent models have stressed the impact of non-aggregated cells on the evolutionary dynamics. We use experimental evolution to explore how selection acting on single-cell adhesion impacts social behaviour. Cell adhesion is held as a fundamental mechanism for cells to direct their cooperative behaviour towards kin, but the way it interplays with social behaviour during evolution has been so far only theoretically explored. Higher levels of cooperation appear to evolve as a result of both increased and decreased cell-substrate adhesion. However, such phenotypes are associated to opposite developmental dynamics in chimeric aggregates. Differences in social behaviour are captured if spore production of isolated strains is also considered, suggesting that in both cases cooperative behaviour is associated to stronger adhesion.