The role of promiscuous molecular recognition in the evolution of self-incompatibility in plants

How do biological networks evolve and expand? We study these questions in the context of the plant collaborative-non-self recognition self-incompatibility system. Self-incompatibility evolved to avoid self-fertilization among plants, which could lead to inviable offspring, (‘inbreeding depression’). Self-incompatibility relies on specific molecular recognition between highly diverse proteins of two families: female and male determinants, such that the combination of genes an individual possesses determines its mating partners. Although a few dozen mating specificities are known from population surveys, previous models struggled to pinpoint the evolutionary trajectories by which new specificities evolved. Here, we construct a novel theoretical framework, that crucially affords interaction promiscuity and multiple distinct partners per protein, as is seen in empirical findings. We find two behavioral regimes of the system. In one regime, we demonstrate spontaneous self-organization of the population into distinct 'classes' with full between-class compatibility and a dynamic long-term balance between class emergence and decay. In the other regime the population is fully self-compatible, namely all individuals are capable of self-fertilization. The choice of either regime depends on the promiscuity and inbreeding depression parameter values.

Our work highlights the importance of molecular recognition promiscuity to network evolvability. Promiscuity was found in additional systems suggesting that our framework could be more broadly applicable.