Abstract

Summary The tropical Andes of South America, the world's richest biodiversity hotspot, are home to many rapid radiations. While geological, climatic, and ecological processes collectively explain such radiations, their relative contributions are seldom examined within a single clade.We explore the contribution of these factors by applying a series of diversification models that incorporate mountain building, climate change, and trait evolution to the first dated phylogeny of Andean bellflowers (Campanulaceae: Lobelioideae). Our framework is novel for its direct incorporation of geological data on Andean uplift into a macroevolutionary model.We show that speciation and extinction are differentially influenced by abiotic factors: speciation rates rose concurrently with Andean elevation, while extinction rates decreased during global cooling. Pollination syndrome and fruit type, both biotic traits known to facilitate mutualisms, played an additional role in driving diversification. These abiotic and biotic factors resulted in one of the fastest radiations reported to date: the centropogonids, whose 550 species arose in the last 5 million yr.Our study represents a significant advance in our understanding of plant evolution in Andean cloud forests. It further highlights the power of combining phylogenetic and Earth science models to explore the interplay of geology, climate, and ecology in generating the world's biodiversity.

Highlights

  • Species-rich rapid radiations are a conspicuous ecological and evolutionary phenomenon in the Tree of Life

  • We find no evidence that the results are affected by dating method, calibration strategy, or branch length heterogeneity: the 95% credibility intervals (CIs) of the re-estimated ages overlap with the 95% CIs from the BEAST analysis that we use for diversification analyses

  • We modeled the impact of traits on the diversification of Neotropical bellflowers by concurrently estimating their impact on speciation, extinction, and transition rates using binary state-speciation and extinction (BiSSE) (Maddison et al, 2007)

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Summary

Introduction

Species-rich rapid radiations are a conspicuous ecological and evolutionary phenomenon in the Tree of Life. Clades that have undergone such diversification are often documented in insular environments, including islands (Baldwin & Sanderson, 1998; Givnish et al, 2009; Lapoint et al, 2014), lakes (Wagner et al, 2012), and mountains (McGuire et al, 2007; Hoorn et al, 2013; Hughes & Atchison, 2015; Merckx et al, 2015) They represent just one-eighth of terrestrial land surface, mountains are home to one-third of all species (Antonelli, 2015) and a large number of species-rich radiations (Hughes & Atchison, 2015; Schwery et al, 2015), including some of the fastest diversification rates reported to date (Madrin~an et al, 2013). Of particular importance are the tropical Andes, which stretch from Venezuela to northern Argentina along the western coast of South America These incredibly species-rich mountains (Barthlott et al, 2005; Kreft & Jetz, 2007) are home to c. The extent of this biodiversity is especially striking considering the recency of mountain uplift: despite debate over the precise timing and rates of uplift (Sempere et al, 2006; Ehlers & Poulsen, 2009), an increasing body of evidence suggests that

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