Ecological advantages and evolutionary limitations of aggregative multicellular development

All multicellular organisms develop through one of two basic routes: they either aggregate from free-living cells, creating potentially-chimeric multicellular collectives, or they develop clonally via mother-daughter cellular adhesion. While evolutionary theory makes clear predictions about trade-offs between these developmental modes, these have never been experimentally tested in otherwise genetically-identical organisms. We engineered unicellular baker’s yeast (Saccharomyces cerevisiae) to develop either clonally (‘snowflake’, Δace2), or aggregatively (‘floc’,GAL1p::FLO1), and examined their fitness in a fluctuating environment characterized by periods of growth and selection for rapid sedimentation. When cultured independently, aggregation was far superior to clonal development, providing a 35% advantage during growth, and a 2.5-fold advantage during settling selection. Yet when competed directly, clonally-developing snowflake yeast rapidly displaced aggregative floc. This was due to unexpected social exploitation: snowflake yeast, which do not produce adhesive FLO1, nonetheless become incorporated into flocs at a higher frequency than floc cells themselves. Populations of chimeric clusters settle much faster than floc alone, providing snowflake yeast with a fitness advantage during competition. Mathematical modeling suggests that such developmental cheating may be difficult to circumvent; hypothetical ‘choosy floc’ that avoid exploitation by maintaining clonality pay an ecological cost when rare, often leading to their extinction. Our results highlight the conflict at the heart of aggregative development: non-specific cellular binding provides a strong ecological advantage – the ability to quickly form groups – but this very feature leads to its exploitation.