<p>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. It relies on specific molecular recognition between highly diverse proteins expressed in the female and male reproductive organs, such that the combination of proteins an individual possesses determines its mating partners, defining distinct ‘mating specificities’. Although a few dozen mating specificities are known from population surveys, previous models struggled to pinpoint the evolutionary trajectories by which new specificities evolved. We construct a novel theoretical framework, synthesizing evolutionary and biophysical models, that crucially affords interaction promiscuity and multiple distinct partners per protein, as is seen in empirical findings. 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.</p><p>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.</p><p> </p><p><strong>FOR THE LATEST UPDATES AND CONTENT ON SOFT MATTER AND BIOLOGICAL PHYSICS AT THE WEIZMANN, VISIT OUR WEBSITE: https://www.biosoftweizmann.com/</strong></p><p> </p><p> </p>