Tracing the impact of the Andean uplift onNeotropical plant evolutionAlexandre Antonellia,1,2, Johan A. A. Nylanderb, Claes Perssona, and Isabel Sanmartı´nc,2aDepartment of Plant and Environmental Sciences, University of Gothenburg, Box 461, 405 30 Gothenburg, Sweden;bDepartment of Botany, StockholmUniversity, 106591 Stockholm, Sweden; andcDepartment of Biodiversity and Conservation, Real Jardı´n Bota´ nico, Consejo Superior de InvestigacionesCientificas, Plaza de Murillo 2, 28014 Madrid, SpainEdited by Bruce H. Tiffney, University of California, and accepted by the Editorial Board April 13, 2009 (received for review November 11, 2008)Recent phylogenetic studies have revealed the major role playedby the uplift of the Andes in the extraordinary diversification of theNeotropical flora. These studies, however, have typically consid-ered the Andean uplift as a single, time-limited event fostering theevolution of highland elements. This contrasts with geologicalreconstructions indicating that the uplift occurred in discrete pe-riods from west to east and that it affected different regions atdifferent times. We introduce an approach for integrating Andeantectonics with biogeographic reconstructions of Neotropicalplants, using the coffee family (Rubiaceae) as a model group. Thedistribution of this family spans highland and montane habitats aswell as tropical lowlands of Central and South America, thusoffering a unique opportunity to study the influence of the Andeanuplift on the entire Neotropical flora. Our results suggest that theRubiaceae originated in the Paleotropics and used the boreotro-pical connection to reach South America. The biogeographic pat-terns found corroborate the existence of a long-lasting dispersalbarrier between the Northern and Central Andes, the ‘‘WesternAndean Portal.’’ The uplift of the Eastern Cordillera ended thisbarrier, allowing dispersal of boreotropical lineages to the South,but gave rise to a huge wetland system (‘‘Lake Pebas’’) in westernAmazonia that prevented in situ speciation and floristic dispersalbetween the Andes and Amazonia for at least 6 million years. Here,we provide evidence of these events in plants.biogeography 兩 Neotropical biodiversity 兩 RubiaceaeThe uplif t of the tropical Andes in the Neogene had aprofound impact on the history of the South Americanc ontinent. It changed the course of the Amazon system fromflowing northwest wards to the modern system that flows to theAtlantic side (1, 2) and affected the climate of the region byfor ming the only barrier to atmospheric circulation in theSouthern Hemisphere (3). Recent phylogenetic studies haveshown that the Andean orogeny had also a major role in theevolution of the Neotropical flora. The Neotropics hold thehighest plant species diversity in the world (4). This richness hastraditionally been explained in terms of environmental factors(5), but lately, more integrative explanations have been advancedthat emphasize the role of historical and evolutionary factors inthe shaping of Neotropical diversity (6, 7). The ‘‘tropical con-servatism hypothesis,’’ for example, argues that there are moreplant species in the Neotropics simply because more lineagesoriginated and diversified there, owing to the long-term climaticst ability of the region and the tendency of species to retain theirclimatic niches over evolutionary time (7, 8). It is now also clearthat part of this richness has been gained by the mig ration oflineages from other biogeog raphic regions (6). For instance,pantropically distributed plant families such as Malpighiaceae,Fabaceae, and Annonaceae (6, 9, 10, 11) originated at temperatelatitudes as part of the for mer ‘‘boreotropical flora’’ (12–14) andsubsequently entered the Neotropics via the mountain ranges ofCentral America and the newly formed Northern A ndes. Onepoint in common to these hypotheses is the key role that thefor mation of the tropical Andes would have played in thehistorical diversification of the Neotropical flora (15). Recentphylogenetic studies have shown that the Andean uplift actedboth as a dispersal route for boreotropical lineages (16, 17) andas a driver in promoting rapid diversification, via allopatricspeciation and ecological displacement, in highland (16–19) andmont ane (11) habit ats.Fewer studies, however, have documented the impact of theA ndean uplift on the lowland Amazonian flora. Clearly, theuplif t must have affected these taxa by forming a new bioticbarrier and profoundly changing the hydrology and climate ofthe region (20). Furthermore, previous biogeographic studies onA ndean radiations have typically considered the Andean orog-eny as a single, time-limited event, usually in connection with thefinal (Miocene to Pleistocene) uplift of the A ndes (11, 19). Thisc ontrasts with geological reconstructions indicating that theuplif t took place in discrete periods, progressing from south tonorth and from west to east and af fecting different regions atdif ferent times (2, 3, 21, 22). Episodic marine incursions, relatedto global sea level rises during the extensional tectonic phasesthat followed periods of major uplift, had a dramatic impact inthe drainage patterns of the region, as evidenced by paleogeo-graphic and paleontological evidence (1, 2, 23–28). These marineincursions have been discussed in relation to their role as apathway in the evolutionary transition from marine to freshwaterhabit ats of Neotropical fishes (24, 29), but they c ould also haveacted as barriers to dispersal or as vicariance events fragmentingthe ranges of terrestrial animals and plants. It seems surprisingthat, despite increasingly det ailed geological reconstructions (2,24, 26–28), thus far no study has attempted to document theef fect of these events on the evolution of the Neotropical flora.Generally, det ailed reconstr uctions have been hampered by thelack of resolution in many Andean species-rich clades (19).Current biogeographic methods require well-resolved phylog-en ies, and uncertainty in phylogenetic relationships makes itdif ficult to reconstruct the specific sequence of geological vi-cariance and speciation events.Here, we use an integration of phylogenetic, biogeographic,and molecular dating methods to reconstruct the evolutionaryhistory of tribes Cinchoneae and Isertieae, which together formone of the major clades of Neotropical Rubiaceae. The distri-Author contributions: A.A. and I.S. designed research; A.A.
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