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Among the fundamental questions regarding cultivated plants is their geographic origin and region of domestication. The genus Cucumis, which includes cucumber (Cucumis sativus) and melon (Cucumis melo), has numerous wild African species, and it has therefore been assumed that melon originated in Africa. For cucumber, this seemed less likely because wild cucumbers exist in India and a closely related species lives in the Eastern Himalayas. Using DNA sequences from plastid and nuclear markers for some 100 Cucumis accessions from Africa, Australia, and Asia, we show here that melon and cucumber are of Asian origin and have numerous previously overlooked species-level relatives in Australia and around the Indian Ocean. The wild progenitor of C. melo occurs in India, and our data confirm that the Southeast Asian Cucumis hystrix is the closest relative of cucumber. Most surprisingly, the closest relative of melon is Cucumis picrocarpus from Australia. C. melo diverged from this Australian sister species approximately 3 Ma, and both diverged from the remaining Asian/Australian species approximately 10 Ma. The Asian/Australian Cucumis clade comprises at least 25 species, nine of them new to science, and diverged from its African relatives in the Miocene, approximately 12 Ma. Range reconstruction under maximum likelihood suggests Asia as the ancestral area for the most recent common ancestor of melon and cucumber, fitting with both having progenitor populations in the Himalayan region and high genetic diversity of C. melo landraces in India and China. Future investigations of wild species related to melon and cucumber should concentrate on Asia and Australia.

Background: Melon, Cucumis melo, and cucumber, C. sativus, are among the most widely cultivated crops worldwide. Cucumis, as traditionally conceived, is geographically centered in Africa, with C. sativus and C. hystrix thought to be the only Cucumis species in Asia. This taxonomy forms the basis for all ongoing Cucumis breeding and genomics efforts. We tested relationships among Cucumis and related genera based on DNA sequences from chloroplast gene, intron, and spacer regions (rbcL, matK, rpl20-rps12, trnL, and trnL-F), adding nuclear internal transcribed spacer sequences to resolve relationships within Cucumis., Results: Analyses of combined chloroplast sequences (4,375 aligned nucleotides) for 123 of the 130 genera of Cucurbitaceae indicate that the genera Cucumella, Dicaelospermum, Mukia, Myrmecosicyos, and Oreosyce are embedded within Cucumis. Phylogenetic trees from nuclear sequences for these taxa are congruent, and the combined data yield a well-supported phylogeny. The nesting of the five genera in Cucumis greatly changes the natural geographic range of the genus, extending it throughout the Malesian region and into Australia. The closest relative of Cucumis is Muellerargia, with one species in Australia and Indonesia, the other in Madagascar. Cucumber and its sister species, C. hystrix, are nested among Australian, Malaysian, and Western Indian species placed in Mukia or Dicaelospermum and in one case not yet formally described. Cucumis melo is sister to this Australian/Asian clade, rather than being close to African species as previously thought. Molecular clocks indicate that the deepest divergences in Cucumis, including the split between C. melo and its Australian/Asian sister clade, go back to the mid-Eocene., Conclusion: Based on congruent nuclear and chloroplast phylogenies we conclude that Cucumis comprises an old Australian/Asian component that was heretofore unsuspected. Cucumis sativus evolved within this Australian/Asian clade and is phylogenetically far more distant from C. melo than implied by the current morphological classification.