Genomic evidence for supergene control of Darwin’s “complex marriage arrangement” – the tristylous floral polymorphism

Tristyly is a polymorphism characterized by three flower morphs with reciprocal stigma and anther heights controlled by two epistatically interacting diallelic loci ( S and M ), hypothesized to be supergenes. Chromosome-level genome assemblies of Eichhornia paniculata identified the S- and M- loci. The S -locus is a supergene consisting of two divergent alleles: The S -allele (2.51Mb) with three S -allele specific genes hemizygous in most S-morph plants and the s -allele (596kb) with five s -allele specific genes. Two of the S -allele specific genes, LAZY1-S and HRGP-S, were specifically expressed in styles and stamens, respectively, making them tristyly candidate genes. The M -locus contained one gene (LAZY1-M), homologous to LAZY1-S, that was present in the M -allele but absent from the m -allele. Estimates of allele ages are consistent with the prediction that the S- locus evolved before the M -locus. Re-use of the same gene family highlights the potential role of gene duplication in the evolution of epistatic multilocus polymorphisms.