Climatic and biogeographic processes underlying the diversification of the pantropical and early divergent angiosperm family Annonaceae

Abstract

AimTropical rainforests harbour the richest biodiversity among terrestrial ecosystems, but few studies have addressed underlying processes of species diversification in these ecosystems. We use the pantropical and early divergent flowering plant family Annonaceae as a model system to investigate how abiotic factors such as climate and biogeographic events contribute to the diversification process and lead to its high diversity across a long evolutionary history. LocationTropics and subtropics TaxonAnnonaceae MethodsA super-matrix was constructed for 835 taxa (34% of Annonaceae species), based on eight chloroplast regions. To understand the patterns of diversification, we reconstructed climatic niche evolution and historical biogeographical events, and tested their association with diversification rates. ResultsThe analysis of temperature-dependent models in Annonaceae lineages provides strong support for the significant influence of global temperature on net diversification and accumulation of species diversity. The pattern of lineage accumulation in the initial radiation is better aligned with the "museum model," followed by later accumulation consistent with the "recent cradle model" from the late Oligocene to the present. The increase in the diversification rate of the family (around 25 Ma) lags behind the accumulation of niche divergences (around 15 Ma). Biogeographic events are related to only two of the five diversification rate shifts detected. While no direct relationship to shifts in the diversification rate was uncovered, shifts in niche evolution appear to be associated with increasingly seasonal environments. Main ConclusionsGlobal temperature plays a crucial role in driving recent rapid diversification in the Annonaceae. Our study challenges the prevailing assumption of the "museum model" alone and proposes instead a transition from the "museum model" to the "recent cradle model" during the diversification history of the family. However, our findings do not support the direct correlation of any particular climatic niche shifts or historical biogeographical events with shifts in diversification rate. Instead, Annonaceae diversification can lead to later niche divergence as a result of increasing interspecific competition arising from species accumulation. The evolutionary direction of niche shifts furthermore provides insight into the future expansion of Annonaceae into temperate regions. Our results highlight the complexity of the diversification process in taxa with long evolutionary histories, indicating that identifying isolated driving factors is simplistic and inadequate for explaining the observed patterns. Further comprehensive analyses of range evolution are necessary to delve deeper into the interplay among key opportunities, key innovation, and species diversification.