The transition from combined to separate sexes in plants drives genomic change, from recombination suppression at sex-determining loci to shifts in selection across autosomes and cytoplasmic genomes. In Amaranthus, a genus that includes ancient grain crops and noxious weeds, separate sexes arose twice through non-homologous sex-determining architectures, with at least one reversion to monoecy, yet plastid and mitochondrial phylogenies group the two dioecious lineages together despite independent origins. The source of this discordance and whether independent origins of dioecy produced parallel or lineage-specific genomic responses remain unknown. We sampled nuclear, plastid, and mitochondrial genomes across 19 species, resolving the backbone phylogeny of the genus and dating the crown to 2--5~Ma. Coalescent simulations rejected incomplete lineage sorting in favor of multiple organelle capture events, implying historical exchange across reproductive barriers separating the two dioecious clades. Nuclear allele sharing was concentrated within each dioecious clade rather than between them, consistent with recombination eroding nuclear donor ancestry while captured cytoplasmic genomes persist. Dioecy was associated with genome-wide shifts in selection intensity, with positive selection concentrated on the stems of each dioecious clade but targeting largely non-overlapping genes and leaving little signature within sex-determining regions. Plastid coding sequences evolved under relaxed purifying selection, and nuclear-encoded plastid-targeted genes were enriched for episodic positive selection, consistent with compensatory cytonuclear evolution. The probable reversion to monoecy in A. pumilus, within a lineage shaped by repeated organelle capture, raises the possibility that hybridization and the lability of separate sexes are connected in this group.
Timerman, D., Leung, J., Eaton, D. A. R.
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