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Premise of the study: The opuntias (nopales, prickly pears) are not only culturally, ecologically, economically, and medicinally important, but are renowned for their taxonomic difficulty due to interspecific hybridization, polyploidy, and morphological variability. Evolutionary relationships in these stem succulents have been insufficiently studied; thus, delimitation of Opuntia s.s. and major subclades, as well as the biogeographic history of this enigmatic group, remain unresolved.

Methods: We sequenced the plastid intergenic spacers atpB-rbcL, ndhF-rpl32, psbJ-petA, and trnL-trnF, the plastid genes matK and ycf1, the nuclear gene ppc, and ITS to reconstruct the phylogeny of tribe Opuntieae, including Opuntia s.s. We used phylogenetic hypotheses to infer the biogeographic history, divergence times, and potential reticulate evolution of Opuntieae.

Key results: Within Opuntieae, a clade of Tacinga, Opuntia lilae, Brasiliopuntia, and O. schickendantzii is sister to a well-supported Opuntia s.s., which includes Nopalea. Opuntia s.s. originated in southwestern South America (SA) and then expanded to the Central Andean Valleys and the desert region of western North America (NA). Two major clades evolved in NA, which subsequently diversified into eight subclades. These expanded north to Canada and south to Central America and the Caribbean, eventually returning back to SA primarily via allopolyploid taxa. Dating approaches suggest that most of the major subclades in Opuntia s.s. originated during the Pliocene.

Conclusions: Opuntia s.s. is a well-supported clade that includes Nopalea. The clade originated in southwestern SA, but the NA radiation was the most extensive, resulting in broad morphological diversity and frequent species formation through reticulate evolution and polyploidy.