Fate of a supergene in the shift from diploidy to polyploidy

Abstract

Despite the evolutionary importance of supergenes, their properties in polyploids remain unexplored. Polyploid genomes are expected to undergo chromosomal rearrangements and gene losses over time, potentially affecting supergene architecture. The iconic distyly supergene (S-locus), controlling a floral heteromorphism with two self-incompatible morphs, has been well-documented in diploids, but remains unknown in polyploids. Primula, the classic model for distyly since Darwin, is ancestrally diploid and distylous, yet polyploid, homostylous species with a single, self-compatible floral morph evolved repeatedly. The intraspecific loss of distyly is associated with small loss-of-function mutations in the S-locus CYPT gene controlling style length and female self-incompatibility. Over longer timescales, relaxed selection on CYPT should generate greater accumulation of larger mutations, including exon and gene loss. By analyzing the first assembled genome of an allotetraploid, homostylous species (Primula grandis) in a comparative framework, we discovered two, nearly identical S-locus alleles in the same subgenome, suggesting it originated via inter-specific hybridization between a homostylous and a distylous progenitor. Conformant to predictions from theory, the macroevolutionary loss of distyly coincided with considerable degeneration of CYPT, while other S-locus genes remained largely unaffected, suggesting the shift to homostyly preceded and facilitated polyploid establishment. At the whole-genome level, we found minimal subgenome dominance -- as expected, given the inferred recent origin of P. grandis -- and highly reduced genetic diversity, congruently with its narrow distribution and self-compatibility. This study provides the first comparison of a supergene across ploidy levels and reproductive systems, contributing new knowledge on the previously unknown fate of supergenes in polyploids. SIGNIFICANCEThis study advances knowledge on genome evolution by elucidating how supergenes (clusters of tightly linked genes) evolve across species with different sets of chromosomes and reproductive systems. By analyzing the newly assembled genome of the polyploid, self-compatible Primula grandis in a broad framework, we provide the first comparison of the distyly supergene between diploid outcrossers and polyploid self-fertilizers. We discovered one pair of identical supergene alleles in the same subgenome, rather than one pair per subgenome, revealing the species originated via a cross between a self-compatible and a self-incompatible progenitor. Conformant to theory, the gene controlling female self-incompatibility and style length (CYPT) was considerably degenerated, because of relaxed selection over time, with the rest of the supergene largely unaffected.