The role of the unicellular bottleneck and organism size in mediating cooperation and conflict among cells at the onset of multicellularity

Abstract

Evolutionary transitions in individuality introduce new levels of selection and thus enable discordant selection, threatening the stability of the transition. Cancer is such a problem for multicellularity. So why have so many transitions to multicellularity persisted? One possibility is that the unicellular propagule maintains cooperation among cells by purging cheaters. The evolution of propagule size has been modeled previously, but in the absence of competition between individuals, which may often select for larger propagules. How does the nature of competition between individuals affect the optimal propagule size in the presence of cancer? Here we take a model of early multicellularity, add cancer, and simulate size-dependent competition on a lattice, which allows us to tune the strength of interspecific vs. intraspecific competition via dispersal. As expected, cancer favours strategies with unicellular propagules while size-dependent competition favours strategies with few large propagules (binary fragmentation). How these opposing forces resolve depends on dispersal. Local dispersal, which intensifies intraspecific competition, favours binary fragmentation, which reduces intraspecific competition for space, with one unicellular propagule. Global dispersal instead favours multiple fission when cancer is common. Our results shed light on the evolution of multicellular life cycles and the prevalence of unicellular propagules across the tree of