Long-distance dispersals and ecological transitions underlie the biogeographic expansion of the pantropical magnoliid genus Xylopia (Annonaceae)

Pantropical taxa with broad and changing distributions provide useful models for assessing drivers of tropical tree biodiversity. Originating at the Eocene-Oligocene boundary, Xylopia is a vertebrate-dispersed woody plant genus with ca. 190 species evenly distributed across the Tropics. How did biogeographic and ecological transitions in this genus shape its broad present-day distribution? We analysed these transitions using ancestral area, climatic and spatial phylogenetic reconstructions, based on an extensive nuclear phylogeny and a curated dataset of occurrence records. The ancestral area was reconstructed as palaeotropical. The genus then underwent two dispersals from Africa, one to the Asia-Pacific area and one to the Neotropics. While niche conservatism in continental rain forests continued, the genus repeatedly transitioned to subhumid, inundated and ultramafic environments. Transitions from rain forests to subhumid environments increased in the Afrotropics as many rain forest groups underwent extinction. Association with inundated habitats, frequent in the early evolution of the genus, became sporadic. Ultramafic transitions occurred in five clades. Xylopia is present on 51 tropical islands; single-island endemics make up ca. 90% of insular species. Repeated dispersals took place between Africa and Madagascar, the Sunda and Sahul plates in the Asia-Pacific and from Central America to the Caribbean. Island distributions indicate overdispersion to remote islands, as well as limited radiations and stepping-stone dispersals. Novel environments, including islands, acted largely as sinks, together encompassing about half the species in the genus. A suite of traits promoting long-distance dispersal by a variety of non-resident birds, combined with the capacity for habitat transitions, were fundamental drivers of pantropical expansion and diversification. These drivers operated repeatedly in all regions, while idiosyncratic historical factors determined the timing and routes of dispersals. Age and distribution of basal grade lineages suggest that the ancestral Xylopia lineage occupied Eocene Boreotropical forests, moving southwards and diversifying independently in the Afrotropic and Asia-Pacific areas of the Palaeotropics. Biogeographic stochastic mapping estimated high regional in situ speciation (89.8%) amongst total biogeographic events for Xylopia . The plants provide high value seed rewards taken by birds that transit long distances and between habitats, promoting long-distance dispersal. Xylopia exhibits overdispersion even to isolated islands, but there is no significant correlation between species richness and isolation index. In response to Miocene aridification and shifts to monsoon climates in the Afrotropics, Xylopia dispersed across multiple lineages, including transitions to subhumid habitats. Ultramafic species occur on islands throughout the range of Xylopia ; radiations took place in Xylopia sect. Xylopia on Cuba and in Xylopia sect. Stenoxylopia on New Guinea and New Caledonia.