The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae) Laura Lagomarsino, Fabien L. Condamine, Alexandre Antonelli, Andreas Mulch, Charles C. Davis To cite this version: Laura Lagomarsino, Fabien L. Condamine, Alexandre Antonelli, Andreas Mulch, Charles C. Davis. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytologist, Wiley, 2016, 210 (4), pp.1430-1442. 10.1111/nph.13920. hal-03048137 HAL Id: hal-03048137 https://hal.archives-ouvertes.fr/hal-03048137 Submitted on 9 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Research The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae) Laura P. Lagomarsino1, Fabien L. Condamine2, Alexandre Antonelli2,3, Andreas Mulch4,5 and Charles C. Davis1 1Department of Organismic and Evolutionary Biology, Harvard University Herbaria, Harvard University, Cambridge, MA 02138, USA; 2Department of Biological and Environmental Sciences, University of Gothenburg, Goteborg€ SE 405 30, Sweden; 3Gothenburg Botanical Garden, Goteborg€ SE 413 19, Sweden; 4Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberg, Frankfurt/Main 60325, Germany; 5Institute for Geosciences, Goethe University Frankfurt, Frankfurt/Main 60438, Germany Summary Author for correspondence: The tropical Andes of South America, the world’s richest biodiversity hotspot, are home to Laura P. Lagomarsino many rapid radiations. While geological, climatic, and ecological processes collectively explain Tel: +1 314 577 0285 such radiations, their relative contributions are seldom examined within a single clade. Email: [email protected] We explore the contribution of these factors by applying a series of diversification models Received: 27 October 2015 that incorporate mountain building, climate change, and trait evolution to the first dated phy- Accepted: 26 January 2016 logeny of Andean bellflowers (Campanulaceae: Lobelioideae). Our framework is novel for its direct incorporation of geological data on Andean uplift into a macroevolutionary model. New Phytologist (2016) 210: 1430–1442 We show that speciation and extinction are differentially influenced by abiotic factors: spe- doi: 10.1111/nph.13920 ciation rates rose concurrently with Andean elevation, while extinction rates decreased during global cooling. Pollination syndrome and fruit type, both biotic traits known to facilitate mutu- Key words: Andes, biodiversity hotspot, alisms, played an additional role in driving diversification. These abiotic and biotic factors climate change, diversification, Lobelioideae, resulted in one of the fastest radiations reported to date: the centropogonids, whose 550 Neotropics, pollination syndromes, rapid species arose in the last 5 million yr. radiation. 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. > 60% of the current elevation of the central Andes was attained Introduction within the last 10 million yr (Myr) (Gregory-Wodzicki, 2000; Species-rich rapid radiations are a conspicuous ecological and Garzione et al., 2006, 2008, 2014). Although the onset of evolutionary phenomenon in the Tree of Life. Clades that have Andean orogeny dates to the Paleocene and Eocene (66– undergone such diversification are often documented in insular 33.9 Myr), including in regions as far north as the modern East- environments, including islands (Baldwin & Sanderson, 1998; ern Cordillera of Colombia (Parra et al., 2009), exceptionally Givnish et al., 2009; Lapoint et al., 2014), lakes (Wagner et al., rapid surface uplift occurred during the late Miocene (c. 10– 2012), and mountains (McGuire et al., 2007; Hoorn et al., 2013; 6 Myr) and early Pliocene (c. 4.5 Myr) (Garzione et al., 2008; Hughes & Atchison, 2015; Merckx et al., 2015). Although they Hoorn et al., 2010; Mulch et al., 2010). Such mountain building represent just one-eighth of terrestrial land surface, mountains is thought to promote diversification in a variety of ways, includ- are home to one-third of all species (Antonelli, 2015) and a large ing by increasing physiographic heterogeneity, affecting local and number of species-rich radiations (Hughes & Atchison, 2015; regional climate, facilitating the immigration of preadapted Schwery et al., 2015), including some of the fastest diversification species, and creating opportunities for extensive, parallel geo- rates reported to date (Madrin~an et al., 2013). Of particular graphic speciation and adaptive radiation in island- and importance are the tropical Andes, which stretch from Venezuela archipelago-like venues (Hoorn et al., 2013; Givnish et al., 2014; to northern Argentina along the western coast of South America. Mulch, 2016). These incredibly species-rich mountains (Barthlott et al., 2005; The role of the rise of the Andes in the origination of biodiver- Kreft & Jetz, 2007) are home to c. 15% of all flowering plant sity has been implicated in clades as diverse as birds (McGuire species, half of which are endemic to the region (Myers et al., et al., 2014), butterflies (Elias et al., 2009), and angiosperms 2000). The extent of this biodiversity is especially striking consid- (Hughes & Eastwood, 2006; Madrin~an et al., 2013). Within ering the recency of mountain uplift: despite debate over the pre- angiosperms, previous work has emphasized that the timing cise timing and rates of uplift (Sempere et al., 2006; Ehlers & and geotemporal trajectories of diversification have been very Poulsen, 2009), an increasing body of evidence suggests that different across Andean biomes (Pennington et al., 2010). While 1430 New Phytologist (2016) 210: 1430–1442 Ó 2016 The Authors www.newphytologist.com New Phytologist Ó 2016 New Phytologist Trust This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. New Phytologist Research 1431 high-elevation grassland clades are exceptionally young, fast, and interactions: fruit type and floral morphology. Abiotically dis- species-rich (e.g. Hughes & Eastwood, 2006), clades in lower- persed capsules characterize c. 40% of the species, while the elevation dry inter-Andean valleys are much older, slower, and remaining species produce fleshy, animal-dispersed berries, which species-poor (S€arkinen et al., 2012). Despite their species rich- evolved at least seven times from capsular-fruited ancestors ness, however, cloud forest biomes have been largely unexplored (Lagomarsino et al., 2014). Floral morphology is also highly vari- with respect to angiosperm diversification, although data suggest able. Lysipomia produces small, white flowers indicative of inver- that they are intermediate in terms of age and tempo (S€arkinen tebrate pollination (Faegri & van der Pijl, 1979), while both the et al., 2012). Chilean lobelias and the centropogonids produce robust flowers Identifying the causes of species-rich rapid radiations, such as that are usually vertebrate-pollinated. Flowers in the centropogo- those that characterize Andean high-elevation grasslands and nid clade are particularly diverse (Fig. 2) and principally adapted cloud forests, is a major goal in ecology and evolutionary biology. to pollination by hummingbirds and nectar bats (Colwell et al., While rapid diversification is undoubtedly the product of both 1974; Stein, 1992; Muchhala, 2006; Muchhala & Potts, 2007). abiotic and biotic factors acting on different spatial and temporal Owing to their broad Andean distribution and remarkable flo- scales (Antonelli & Sanmartın, 2011; Ezard et al., 2011; Bouch ral and fruit diversity, the Neotropical bellflowers represent a enak-Khelladi et al., 2015), a tendency to explain a given diversity model group to examine the interaction of abiotic and biotic fac- pattern with a single process has persisted until recently. For tors that trigger mountain radiations. To accomplish this goal, montane Andean radiations, this was exemplified by invoking we develop and apply numerous statistical models to investigate molecular divergence time estimates contemporaneous with the diversification dynamics in the Neotropical bellflowers. More- final stages of Andean uplift, during which new habitats formed over, our analyses are among the first to incorporate geological and provided ecological opportunity for diversification (Hughes data into a model of evolutionary diversification (also see Valente & Eastwood, 2006; McGuire et al., 2014). However, other fac- et al., 2014 and Mulch, 2016). In this framework, we explicitly tors are probably at play simultaneously. For example, rapid plant investigate the influence of geology, climate, and ecological traits diversification in the