• Cooperation;
  • intragenomic conflict;
  • mutualism;
  • partner fidelity;
  • permanent translocation heterozygosity

Recombination is a powerful policing mechanism to control intragenomic cheats. The “parliament of the genes” can often rapidly block driving genes from cheating during meiosis. But what if the genome parliament is reduced to only two members, or supergenes? Using a series of simple game-theoretic models inspired by the peculiar genetics of Oenothera sp., we illustrate that a two supergene genome (α and β) can produce a number of surprising evolutionary dynamics, including increases in lineage longevity following a transition from sexuality (outcrossing) to asexuality (clonal self-fertilization). We end by interpreting the model in the broader context of the evolution of mutualism, which highlights that greater α, β cooperation in the self-fertilizing model can be viewed as an example of partner fidelity driving multilineage cooperation.