Phylogenomics of the Olea europaea complex using 15 whole genomes supports recurrent genetic admixture together with differentiation into seven subspecies

BACKGROUND: The last taxonomic account of Olea recognises six subspecies within Olea europaea L., including the Mediterranean olive tree (subsp. europaea) and five other subspecies (laperrinei, guanchica, maroccana, cerasiformis, and cuspidata) distributed across the Old World, including Macaronesian islands. The evolutionary history of this monophyletic group (O. europaea complex) has revealed a reticulated scenario involving hybridization and polyploidization events, leading to the presence of a polyploid series associated with the subspecies. However, how the polyploids originated, and how the different subspecies contributed to the domestication of the cultivated olive are questions still debated. Tracing the recent evolution and genetic diversification of the species is key for the management and preservation of its genetic resources. To study the recent history of the O. europaea complex, we compared newly sequenced and available genomes for 27 individuals representing the six subspecies. RESULTS: Our results show discordance between current subspecies distributions and phylogenomic patterns, which support intricate biogeographic patterns. The subspecies guanchica, restricted to the Canary Islands, is closely related to subsp. europaea, and shows a high genetic diversity. The subsp. laperrinei, restricted now to high mountains of the Sahara desert, and the Canarian subsp. guanchica contributed to the formation of the allotetraploid subsp. cerasiformis (Madeira islands) and the allohexaploid subsp. maroccana (western Sahara region). Our phylogenomic data support the recognition of one more taxon (subsp. ferruginea) for the Asian populations, which is clearly segregated from the African subsp. cuspidata. CONCLUSIONS: In sum, the O. europaea complex underwent several processes of hybridization, polyploidy, and geographical isolation resulting in seven independent lineages with certain morphological traits recognised into subspecies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01583-5.