Phylogenomic analyses in the apple genus Malus s.l. reveal widespread hybridization and allopolyploidy driving the diversifications, with insights into the complex biogeographic history in the Northern Hemisphere

Abstract

Phylogenomic evidence from an increasing number of studies has demonstrated that different data sets and analytical approaches often reconstruct strongly supported but conflicting relationships. In this study, hundreds of single-copy nuclear (SCN) genes (785) and complete plastomes (75) were used to infer the phylogenetic relationships and estimate the historical biogeography of the apple genus Malus sensu lato, an economically important lineage disjunctly distributed in the Northern Hemisphere involved in known and suspected hybridization and allopolyploidy events. The nuclear phylogeny recovered the monophyly of Malus s.l. (including Docynia); however, it was supported to be biphyletic in the plastid phylogeny. An ancient chloroplast capture event best explains the cytonuclear discordance that occurred in the Eocene in western North America. Our conflict analysis demonstrated that ILS, hybridization, and allopolyploidy could explain the widespread nuclear gene tree discordance. We detected one deep hybridization event (Malus doumeri) involving the ancestor of pome-bearing species and Docynia delavayi, and one recent hybridization event (Malus coronaria) between M. sieversii and a combined clade of M. ioensis and M. angustifolia. Furthermore, our historical biogeographic analysis combining living and fossil species supported a widespread East Asian-western North American origin of Malus s.l., followed by a series of extinction events in the Eocene in northern East Aisa and western North America. This study provides a valuable evolutionary framework for the breeding and crop improvement of apples and their close relatives.