Abstract

Supergenes govern multi-trait balanced polymorphisms in a wide range of systems, yet our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in pin and thrum 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 both hemizygous in thrums, but it remains unknown if hemizygosity is pervasive among distyly S-loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. We aimed to characterize 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, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Genomic analyses of additional distylous Linum species further identify shared presence-absence variation at the S-locus, indicating that hemizygosity in thrums is a general feature of Linum S-loci. Finally, we investigate the genetic causes and genomic consequences of breakdown of distyly, resulting in homostylous and largely self-fertilizing species. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes, and shed new light on the evolution and loss of an iconic floral polymorphism.