Balanced polymorphism in a floral transcription factor underlies an ancient rhythm of daily sex alternation in avocado

In avocado and certain wild relatives in Lauraceae, pollination occurs via a synchronized rhythm of floral sex timing between two hermaphroditic flowering types. A-type plants present female-phase flowers in the morning and male-phase flowers in the afternoon, while B-types show the complementary pattern, a form of heterodichogamy. We map this dimorphism in avocado to a genomic region overlapping a single strong candidate gene, <i>SDMYB</i>, where a dominant haplotype confers A-type flowering. <i>SDMYB</i> belongs to a subgroup of R2R3 MYB transcription factors established as key regulators of floral maturation in diverse species with links to circadian jasmonate signaling. Haplotypes at this locus form an ancient trans-species polymorphism maintained by negative frequency-dependent balancing selection over 44 million years, and they segregate in at least 26 non-avocado species, including in a genus where this mating system has not been reported. Across several species examined, rhythmic diel <i>SDMYB</i> expression is associated with biphasic floral anthesis, and the dominant allele, which contains nonsynonymous changes in conserved functional domains, exhibits a <i>cis</i>-regulated phase delay, corresponding to the delayed 2nd anthesis of A-types. The coupling of dichogamy with diel flower movements, widespread among magnoliids, is a likely precursor to daily forms of heterodichogamy. Absence of the <i>SDMYB</i> polymorphism in true cinnamon, which exhibits a highly similar mating system, suggests the possibility that heterodichogamy has convergently evolved within Lauraceae.