Mora-Carrera, E. | bioRxiv Science

bioRxiv2025

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

AO_SCPLOWBSTRACTC_SCPLOWEvolution 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 such repeatability remain poorly understood. Here, by analyzing ten chromosome-scale genome assemblies, including seven newly generated, we discovered that the S-locus supergene (a cluster of tightly linked genes controlling a floral dimorphism called distyly) arose independently multiple times within the primrose family, Darwins iconic system for studying distyly. In each case, the same gene was independently duplicated and co-opted, yet the resulting genomic architectures differed, ranging from hemizygous (present on one chromosome copy) to heterozygous (on both copies). These diverse architectures shaped supergene evolution differently, with genetic degeneration occurring only in the heterozygous case. 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.

evolutionary biology↗

bioRxiv2024

The Primula edelbergii S-locus is an example of a jumping supergene

Research on supergenes, non-recombining genomic regions housing tightly linked genes that control complex phenotypes, has gained prominence in genomics, with supergenes having been described in most eukaryotic lineages. Heterostyly, a floral heteromorphism promoting outcrossing in several angiosperm families, is controlled by the S-locus supergene. Historically, the S-locus has been studied primarily in closely related Primula species and, more recently, in other groups that independently evolved heterostyly. However, it remains unknown whether genetic architecture and composition of the S-locus are maintained among species that share a common origin of heterostyly and subsequently diverged across larger time scales. To address this research gap, we present a chromosome-scale genome assembly of Primula edelbergii, a species that shares the same origin of heterostyly with Primula veris (whose S-locus has been characterized) but diverged from it ca. 18 million years ago. Comparative genomic analyses between P. edelbergii and P. veris allowed us to show, for the first time, that the S-locus can jump (i.e. translocate) between chromosomes. Additionally, we found that four S-locus genes were maintained across time but were reshuffled within the supergene, seemingly without affecting their expression. Furthermore, we confirmed that S-locus hemizygosity counteracts genetic degeneration, otherwise expected in supergenes. Finally, we investigated P. edelbergii evolutionary history within Ericales in terms of whole genome duplications and transposable element accumulation. In summary, our work provides a valuable resource for comparative analyses aimed at investigating the genetics of heterostyly and the pivotal role of supergenes in shaping the evolution of complex phenotypes.

genomics↗