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

Abstract

How do biological networks evolve and expand and which parameters determine their size? 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 hermaphroditic plants. It relies on specific molecular recognition between highly diverse proteins of two families: female and male determinants, such that the combination of alleles an individual possesses determines its mating partners. Though highly diverse, previous models struggled to pinpoint the evolutionary trajectories by which new alleles evolved. Here, we construct a novel theoretical frame-work, that crucially affords interaction promiscuity and multiple distinct partners per protein, empirical findings disregarded by previous models. We demonstrate a dynamic long-term balance between allele emergence and extinction, where their equilibrium number depends on population parameters. 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.