Bread wheat and durum wheat derive from an intricate evolutionary history of three genomes, namely A, B and D, present in both extent diploid and polyploid species. Despite its importance for wheat research, no consensus on the phylogeny of the wheat clade has emerged so far, possibly because of hybridizations and gene flows that make phylogeny reconstruction challenging. Recently, it has been proposed that the D genome originated from an ancient hybridization event between the A and B genomes1. However, the study only relied on four diploid wheat relatives when 13 species are accessible. Using transcriptome data from all diploid species and a new methodological approach, we provide the first comprehensive phylogenomic analysis of this group. Our analysis reveals that most species belong to the D-genome lineage and descend from the previously detected hybridization event, but with a more complex scenario and with a different parent than previously thought. If we confirmed that one parent was the A genome, we found that the second was not the B genome but the ancestor of Aegilops mutica (T genome), an overlooked wild species. We also unravel evidence of other massive gene flow events that could explain long-standing controversies in the classification of wheat relatives. We anticipate that these results will strongly affect future wheat research by providing a robust evolutionary framework and refocusing interest on understudied species. The new method we proposed should also be pivotal for further methodological developments to reconstruct species relationship with multiple hybridizations.

Cultivated wheats are derived from an intricate history of three genomes, A, B, and D, present in both diploid and polyploid species. It was recently proposed that the D genome originated from an ancient hybridization between the A and B lineages. However, this result has been questioned, and a robust phylogeny of wheat relatives is still lacking. Using transcriptome data from all diploid species and a new methodological approach, our comprehensive phylogenomic analysis revealed that more than half of the species descend from an ancient hybridization event but with a more complex scenario involving a different parent than previously thought—Aegilops mutica, an overlooked wild species—instead of the B genome. We also detected other extensive gene flow events that could explain long-standing controversies in the classification of wheat relatives.