J Syst Evol ›› 2021, Vol. 59 ›› Issue (6): 1170-1182.DOI: 10.1111/jse.12688

Special Issue: Virtual Issue to Celebrate the Legacy and Life of Professor Wen-Tsai Wang

• Research Articles • Previous Articles     Next Articles

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

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

  1. 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    2 College of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China
    3 Key Laboratory of Bio‐Resources and Eco‐Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China

    These authors contributed equally to this work.
    *Author for correspondence. E‐mail: hongdy@ibcas.ac.cn
  • Received:2020-04-01 Accepted:2020-09-12 Online:2020-09-17 Published:2021-11-01

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 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.

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