Distinct genomic architectures but the same gene underlie the convergent evolution of a plant supergene.

Abstract

Evolution reflects a balance between innovation and constraint, often repurposing existing components in new contexts. Convergent evolution exemplifies this interplay, with similar traits evolving independently in different species, yet the genomic mechanisms enabling this repeatability remain poorly understood. Here, by analyzing 10 chromosome-scale genome assemblies, including seven newly generated, we found that the <i>S</i>-locus supergene (a cluster of tightly linked genes controlling a floral dimorphism called distyly) arose independently multiple times within the primrose family, Darwin's iconic system for studying distyly. In each case, the same gene was independently duplicated and co-opted. However, the resulting genomic architectures differed, ranging from hemizygous (present on one chromosome copy) to heterozygous (on both copies), challenging the prevailing view that hemizygosity is intrinsic to <i>S</i>-loci and suggesting alternative evolutionary routes to distyly supergene formation. By uncovering multiple mechanisms for supergene origins, our work shows how convergent evolution can produce similar phenotypes by reusing the same genetic building blocks while exploring distinct genomic configurations.