J Syst Evol

• Research Articles •    

Out of the Pan-Himalaya: Evolutionary History of the Paeoniaceae Revealed by Phylogenomics

Shiliang Zhou1,2, Chao Xu1, Jing Liu1, Yan Yu3, Ping Wu1,2, Tao Cheng1, and De-Yuan Hong1*   

  1. 1State Key Laboratory of Systematic & Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    2College of Life Science, University of Chinese Academy of Sciences, Beijing 100043, China
    3Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan 610065, China
  • Received:2020-04-01 Accepted:2020-09-12

Abstract: 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 the Paeoniaceae separated from the other members in Saxifragales in the Campanian of the late Cretaceous, 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. Owing to five vicariance events and 21 dispersal events with territory expansion, 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, P. obovata and P. tenuifolia 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.

Key words: biogeography, molecular dating, Paeonia, phylogeny, reticulate evolution