Premise of the Research: Distyly is a floral polymorphism involving reciprocal herkogamy shaped by selection for pollen transfer efficiency. The variation of the floral organs involved in pollen transfer can be individually affected by environmental and genetic sources of variance, but the organ development will be canalised to minimize reciprocal inaccuracy between anthers and stigmas as this is the focus of selection.Methodology: We measured floral organ and cell length of both morphs of distylous Linum tenue (Linaceae) at different developmental stages of field-and glasshouse-grown plants. We analysed the results to measure reciprocal inaccuracy and identify sources of variance.Pivotal results: Flowers from the field were larger than those from the glasshouse due to both environmental and genetic (population) factors. Pistil and stamen length in adult flowers correlated with flower size, but reciprocal herkogamy was mostly invariant to the size individual floral organs. The length of short floral organs showed greater maladaptive bias, while the length of tall organs showed greater imprecision. During development, the pistils of pin flowers grew at a faster rate than in thrum flowers mostly due to cell elongation, while cell division was more important for male organ height.Conclusions: Distyly in L. tenue involves the interaction of multiple coordinated developmental and environmental mechanisms leading to limited but predictable patterns of variance in the expression of reciprocal herkogamy.
Supergenes govern balanced polymorphisms in a wide range of systems. 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. 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, 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. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes. 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.
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