Phylogenomics of the early-divergent angiosperm family Annonaceae: resolving intertribal and intergeneric relationships in the recalcitrant Malmeoideae subfamily

Abstract

Evolutionary relationships among main lineages of the Annonaceae have become much clearer in recent years. The Annonaceae subfamily Malmeoideae is a dominant component of tropical rainforest in South East Asia and one of the most diverse groups of early angiosperms in the region. The most recent classication of Malmeoideae includes seven tribes: Dendrokingstonieae, Fenerivieae, Maasieae, Malmeeae, Miliuseae, Monocarpieae and Piptostigmateae but relationships among them are still unknown. Miliuseae represents more than 70% of species in Malmeoideae comprising 25 genera and » 510 species of trees and shrubs. The most recent molecular phylogeny of the Miliuseae distinguished 10 well-supported clades based on chloroplast DNA regions. Relationships among the major clades were not supported, and the backbone of the phylogeny remains unresolved. The still poorly resolved phylogeny of tribe Miliuseae represents the largest impediment to understanding broad-scale evolutionary patterns within the family. Here we used phylogenomic approaches in order to resolve the evolutionary relationships among members of two diverse Annonaceae lineages: (1) the seven subtribes in the subfamily Malmeoideae, (2) the 25 genera belonging to the tribe Miliuseae. To answer these questions we used several methodological approaches including different taxon sampling and coverage, the use or exclusion of data partitions and maximum likelihood or Bayesian tree reconstruction. Our data include the first whole chloroplasts genomes sequence for 19 Annonaceae species and previously published species-rich data set with 61 and 5 chloroplast regions for the Malmeoideae. Our results greatly improve phylogenetic reconstruction within Annonaceae and emphasize the importance of experimental methodologies in order to improve phylogenetic signal of NGS data. We report for first time the complete chloroplast sequence for Annonaceae. A large inversion in the large single copy (LSC) region of the chloroplast was detected for all members of the Miliuseae.