Sequential diversification with Miocene extinction and Pliocene speciation linked to mountain uplift explains the diversity of the African rain forest clade Monodoreae (Annonaceae)

Abstract

Abstract Background and Aims Throughout the Cenozoic, Africa underwent several climatic and geological changes impacting the evolution of tropical rain forests (TRFs). African TRFs are thought to have extended from east to west in a ‘pan-African’ TRF, followed by several events of fragmentation during drier climate periods. During the Miocene, climate cooling and mountain uplift led to the aridification of tropical Africa and open habitats expanded at the expense of TRFs, which probably experienced local extinctions. However, in plants, these drivers were previously inferred using limited taxonomic and molecular data. Here, we tested the impact of climate and geological changes on diversification within the diverse clade Monodoreae (Annonaceae) composed of 90 tree species restricted to African TRFs. Methods We reconstructed a near-complete phylogenetic tree, based on 32 nuclear genes, and dated using relaxed clocks and fossil calibrations in a Bayesian framework. We inferred the biogeographical history and the diversification dynamics of the clade using multiple birth–death models. Key Results Monodoreae originated in East African TRFs ~25 million years ago (Ma) and expanded toward Central Africa during the Miocene. We inferred range contractions during the middle Miocene and document important connections between East and West African TRFs after 15–13 Ma. Our results indicated a sudden extinction event during the late Miocene, followed by an increase in speciation rates. Birth–death models suggested that African elevation change (orogeny) is positively linked to speciation in this clade. Conclusion East Africa is inferred as an important source of Monodoreae species, and possibly for African plant diversity in general. Our results support a ‘sequential scenario of diversification’ in which increased aridification triggered extinction of TRF species in Monodoreae. This was quickly followed by fragmentation of rain forests, subsequently enhancing lagged speciation resulting from vicariance and improved climate conditions. In contrast to previous ideas, the uplift of East Africa is shown to have played a positive role in Monodoreae diversification.