Out of the Pan-Himalaya: Evolutionary history of the Paeoniaceae revealed by phylogenomics

Peonies (the Paeoniaceae, Paeonia L.) are famous garden flowers, medicinal plants, and edible oil crops, but their evolutionary history largely remains unknown. To probe into their phylogenetic relationships, evolutionary history, formation of present distribution pattern, and origins of tetraploids, we sequenced 25 fragments belonging to 20 single copy nuclear genes and 14 chloroplast regions of all species in the genus to reconstruct phylogenetic relationships, date the divergence times of lineages, infer the ancestral biogeographical regions, and document the parents of tetraploids. Our results show that Paeoniaceae separated from the other members in Saxifragales in the Campanian of the late Cretaceous and diverged into two clades, woody and herbaceous clades, in the late Oligocene or early Miocene. They survived and early diverged in the Pan-Himalaya where they migrated eastwards to East Asia and further to NW America, and northwards to Middle Asia, and further to Europe. The woody lineage differentiated into two sublineages with accelerated root or floral disk evolution, while the herbaceous lineage diverged into five sublineages. Multiple glacial and interglacial cycles in Europe in the late Pliocene and early Pleistocene created opportunities for the peony species to meet and hybridize in the Mediterranean refugia, giving rise to eight allotetraploid species and four infraspecific tetraploids. Paeonia daurica Andrews, P. obovata Maxim., and P. tenuifolia L. served as the most important parents. The phylogeny of Paeonia L. implies that a new taxonomic system with two subgenera and seven sections should be proposed.