Reconciling conflicting selection pressures in the plant collaborative non-self recognition self-incompatibility system

Complex biological systems should often reconcile conflicting selection pressures. In systems based on molecular recognition, molecules must specifically identify certain partners while excluding others. Here, we study how such selection pressures shape the evolution of the self-incompatibility system in plants. This system inhibits self-fertilization using specific molecular recognition between proteins, expressed in the plant female and male reproductive organs. We study the impact of these opposing selection pressures on the amino acid frequencies in these proteins’ recognition domain. We build on a theoretical framework enabling promiscuous recognition between proteins, as found empirically, and employ stochastic simulations to study their evolution. We find that selection exerts asymmetric responses of amino acid frequencies, affecting female proteins considerably, but hardly the male. Using large deviations theory, we well approximate the simulated frequencies and find agreement with genomic data. Our work offers a general theoretical framework to study the impact of multiple selection pressures, applicable to additional biological systems.