Linum supergene evolution

Supergenes occur in a wide variety of systems, yet our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are hemizygous in thrum individuals. It remains unknown if hemizygosity is pervasive among distyly S-loci and how such regions evolve. Here we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes are major features of the Linum S-locus, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings show remarkable convergence in the genetic architecture of the distyly supergene across widely diverged taxa with independently derived distyly. The chromosome-level genome assembly and detailed characterization of the distyly S-locus in L. tenue will facilitate elucidation of molecular mechanisms underlying the different forms of flowers described by Darwin.