Pleiotropy, cooperation, and the social evolution of genetic architecture

Abstract

Pleiotropy has been suggested as a novel mechanism for stabilising cooperation in bacteria and other microbes. The hypothesis is that linking cooperation with a trait that provides a personal (private) benefit can outweigh the cost of cooperation in situations when cooperation would not be favoured by mechanisms such as kin selection. We analysed the theoretical plausibility of this hypothesis, with analytical models and individual-based simulations. We found that (1) pleiotropy does not stabilise cooperation, unless the cooperative and private traits are linked via a genetic architecture that cannot evolve (mutational constraint); (2) if the genetic architecture is constrained in this way, then pleiotropy favours any type of trait and not especially cooperation; (3) if the genetic architecture can evolve, then pleiotropy does not favour cooperation; and (4) there are several alternative explanations for why traits may be linked, and causality can even be predicted in the opposite direction, with cooperation favouring pleiotropy. Our results suggest that pleiotropy could only explain cooperation under restrictive conditions and instead show how social evolution can shape the genetic architecture.

Author summary

Recent research into microbial communities has revealed that the cooperative secretion of molecules—which are produced by individual cells and benefit neighbouring cells—is linked to the production of privately beneficial intracellular enzymes. This pleiotropic link between commonly and privately beneficial traits has been suggested as a novel way for maintaining cooperation in conditions under which it would otherwise be outcompeted by cheating cells. The reason is that cheats, which do not cooperate, would also lose the benefit of producing the private trait and thus suffer a fitness disadvantage. We test the plausibility of this hypothesis with analytical models and individual-based simulations. We find that cooperation can only be stabilised if one makes restrictive assumptions about the genetic architecture, such that the pleiotropic link with a private trait cannot be broken through further evolution. If the genetic architecture can evolve, then natural selection can favour mutants that do not cooperate but that still perform the private trait, leading to the breakdown of cooperation. We discuss a number of alternative explanations for the observation of linkage between cooperative and private traits and show that causality may even arise in the opposite direction to that previously predicted—when cooperation is favoured, this may select for pleiotropy. Our results suggest a novel explanation for why cooperative and private traits may be linked and show how social evolution can shape the genetic architecture.