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

Abstract

Background and Aims Throughout the Cenozoic, Africa underwent several climatic and geological changes impacting the evolution of tropical rain forests (TRF). African TRF 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 TRF, which likely 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 TRF. 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 biogeographic history and the diversification dynamics of the clade using multiple birth-death models. Key Results Monodoreae originated in East African TRF ca. 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 TRF 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” where increased aridification triggered extinction of TRF species in Monodoreae. This was quickly followed by rain forests fragmentation, 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.

Habitat Opening Fostered Diversity: Impact of Dispersal and Habitat-shifts in the Diversification of a Speciose Afrotropical Insect Group

“…Within this heterogeneous environment, an array of dispersal, vicariance, reverse colonization events, and in situ speciation events within East Africa are inferred during the last 7 million years (Myr) (Figures 1, 3). African highlands (see Appendix S.4.3 for a detailed map) along the Eastern corridor probably acted as altitudinal refugia during the cycles of expansion and contraction of the savannas (Plana 2004;Couvreur et al 2021), resulting in the connection and isolation of related species in highland refugia among both forest-and arid-adapted lineages (Menegon et al 2014, Huntley and Voelker 2017, Portillo et al 2018, Mulvaney et al 2022, Dagallier et al 2023. This hypothesis is supported by: (i) the fact that Sesamiina species endemic to the African highlands belong to distinct lineages (e.g., Se.…”

“…Extensive savannas are distributed around West and Central Africa and extend beyond, forming a belt from West Africa to Southern Africa (Fuchs et al 2011). Allopatric speciation associated with vicariance events resulting from cycles of fragmentation and reconnection of African biomes played a major role in driving species richness in the Afrotropics, especially around the MMCO for forest-adapted species (e.g., Aduse-Poku et al 2022, Dagallier et al 2023. Dispersal events helped shape the diversification of species adapted to open habitats, particularly through the opening of the Eastern arid corridor following the MMCO (e.g., Coleman et al 2003, Sanmartín et al 2010, Kamiński et al 2022.…”