Phylogenomics and historical biogeography of the recalcitrant Annonaceae subfamily Malmeoideae

Abstract

Annonaceae (ca. 2400 species of trees, shrubs and lianas) are characteristic and ecologically important elements in tropical lowland forests of both the Neotropics and the Old World. There have been substantial advances in resolving the backbone phylogeny of the family in recent years, but there are notable exceptions. Intertribal relationships in subfamily Malmeoideae (7 tribes, 47 genera, >770 species) and intergeneric relationships in its largest tribe, Miliuseae (26 genera, ca. 540 species), remain very poorly understood. This has impeded downstream analyses such as investigations of the historical biogeography and character evolution in the family. We used a phylogenomic approach to resolve the relationships in subfamily Malmeoideae. Data from sequencing of total genomic DNA on the Illumina HiSeq2000 platform was used to assemble near-complete plastome DNA sequences. The dataset comprised 55 newly sequenced accessions including samples of all seven tribes and representatives of 45 of 47 currently accepted genera in the subfamily. These data were analysed separately and by inte-grating a supermatrix of previously published DNA data including accessions of all currently accepted genera in Malmeoideae using likelihood and Bayesian phylogenetic reconstruction methods. The resulting phylogenetic reconstructions largely resolve intertribal relationship and intergeneric relationships in tribe Malmeeae, and provide various new insights into intergeneric relationships within tribe Miliuseae. Parts of the Miliuseae backbone, however, remain unresolved. Likelihood ancestral range estimations indicate a wide ancestral distribution for the most recent common ancestor of the Malmeoideae crown group including the Neotropics, Africa and Asia. This is inferred as the result of a range expansion from Africa between the stem and the crown node sometime during a time interval ranging roughly from the mid-Cretaceous to the mid-Eocene. In combination with the fossil record, the results indicate that the ‘boreotropics’, a frost-free and humid climate corridor in the Northern mid-latitudes in the Paleocene-Eocene, likely played an important role facilitating intercontinental dispersal of this group.