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Stubbs, R. L.

Publications and source records attributed to Stubbs, R. L..

3 recordsLinked to original sources

Phenotypic and genomic changes associated with the evolutionary loss of heterostyly in primroses

Trait loss has been documented across broad phylogenetic scales and dissected genetically within species, but how the genetic basis of loss varies among lineages and over evolutionary time remains poorly understood. Heterostyly, a floral polymorphism, represents an ideal case study, as it has been lost repeatedly across angiosperms. In Primula, heterostyly is controlled by the S-locus supergene, and loss-of-function mutations in CYP cause transitions to homostyly. We investigated the critically endangered Primula boveana, whose floral morphology is debated, in the diploid, self-compatible P. sect. Sphondylia. We quantified herkogamy dynamics during anthesis, performed controlled pollination experiments, assembled a chromosome-scale genome, compared S-locus structure and gene expression with heterostylous relatives, and reconstructed phylogenetic relationships within the section. Our results revealed that P. boveana is homostylous, with a disrupted CYP. Herkogamy declines during anthesis, resulting in early anther-stigma contact, autonomous selfing, and reproductive assurance. Thus, unlike other homostylous Primula species, these developmental changes do not represent a delayed selfing strategy. These findings link developmental changes in herkogamy with autonomous selfing and support CYP inactivation as the genetic basis of long homostyly in P. boveana. The extensive degeneration of CYP suggests that prolonged relaxed selection promotes progressive degeneration of non-functional S-genes following heterostyly loss.

evolutionary biology↗

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↗

Fate of a supergene in the shift from diploidy to polyploidy

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.

evolutionary biology↗