A Mixture of “Cheats” and “Co-Operators” Can Enable Maximal Group Benefit

It is commonly assumed that the world would be best off if everyone co-operates. Experimental and mathematical analysis of “co-operation” in yeast show why this isn't always the case.Is a group best off if everyone co-operates? Theory often considers this to be so (e.g. the “conspiracy of doves”), this understanding underpinning social and economic policy. We observe, however, that after competition between “cheat” and “co-operator” strains of yeast, population fitness is maximized under co-existence. To address whether this might just be a peculiarity of our experimental system or a result with broader applicability, we assemble, benchmark, dissect, and test a systems model. This reveals the conditions necessary to recover the unexpected result. These are 3-fold: (a) that resources are used inefficiently when they are abundant, (b) that the amount of co-operation needed cannot be accurately assessed, and (c) the population is structured, such that co-operators receive more of the resource than the cheats. Relaxing any of the assumptions can lead to population fitness being maximized when cheats are absent, which we experimentally demonstrate. These three conditions will often be relevant, and hence in order to understand the trajectory of social interactions, understanding the dynamics of the efficiency of resource utilization and accuracy of information will be necessary.Author Summary: The world is best off, it is usually presumed, when everyone co-operates. However, we discovered in a laboratory experiment involving yeasts that a population can grow more and faster when there is a mix of “cheats” and “co-operators.” In this case “co-operator” cells produce a protein (invertase) that breaks down sugar in the environment enabling it to be used by anyone. “Cheats” eat the broken down sugar but don't produce invertase and so have fewer costs. How can it be that yeast populations do best when such apparently selfish cheats are common? To resolve this we constructed a mathematical model, used this to discover reasons why the classical result wasn't found, and experimentally verified these conclusions. We find three conditions required to recover the unexpected result: (1) the “co-operators” should get more food than “cheats” (e.g. if the two aren't perfectly mixed together), (2) food is used more efficiently when there is a famine than when there is a feast, and (3) the amount of “co-operation” given should not accurately match the amount needed. We argue that all three are likely not to be peculiar to yeast, suggesting that “cheats” may be good for a group in many cases.