Tracing the impact of the Andean uplift on Neotropical plant evolution Alexandre Antonellia 1 2 Johan A A Nylanderb Claes Perssona and Isabel Sanmart nc 2 aDepartment of Plant and Environmental Sciences University of Gothenburg Box 461 405 30 Gothenburg Sweden bDepartment of Botany Stockholm University 106591 Stockholm Sweden and cDepartment of Biodiversity and Conservation Real Jard n Bota nico Consejo Superior de Investigaciones Cientificas Plaza de Murillo 2 28014 Madrid Spain Recent phylogenetic studies have revealed the major role played by the uplift of the Andes in the extraordinary diversification of the Neotropical flora These studies however have typically considered the Andean uplift as a single time limited event fostering the evolution of highland elements This contrasts with geological reconstructions indicating that the uplift occurred in discrete periods from west to east and that it affected different regions at different times We introduce an approach for integrating Andean tectonics with biogeographic reconstructions of Neotropical plants using the coffee family Rubiaceae as a model group The distribution of this family spans highland and montane habitats as well as tropical lowlands of Central and South America thus offering a unique opportunity to study the influence of the Andean uplift on the entire Neotropical flora Our results suggest that the Rubiaceae originated in the Paleotropics and used the boreotropical connection to reach South America The biogeographic patterns found corroborate the existence of a long lasting dispersal barrier between the Northern and Central Andes the Western Andean Portal The uplift of the Eastern Cordillera ended this barrier allowing dispersal of boreotropical lineages to the South but gave rise to a huge wetland system Lake Pebas in western Amazonia that prevented in situ speciation and floristic dispersal between the Andes and Amazonia for at least 6 million years Here we provide evidence of these events in plants biogeography Neotropical biodiversity Rubiaceae T he uplift of the tropical Andes in the Neogene had a profound impact on the history of the South American continent It changed the course of the Amazon system from flowing northwestwards to the modern system that flows to the Atlantic side 1 2 and affected the climate of the region by forming the only barrier to atmospheric circulation in the Southern Hemisphere 3 Recent phylogenetic studies have shown that the Andean orogeny had also a major role in the evolution of the Neotropical flora The Neotropics hold the highest plant species diversity in the world 4 This richness has traditionally been explained in terms of environmental factors 5 but lately more integrative explanations have been advanced that emphasize the role of historical and evolutionary factors in the shaping of Neotropical diversity 6 7 The tropical conservatism hypothesis for example argues that there are more plant species in the Neotropics simply because more lineages originated and diversified there owing to the long term climatic stability of the region and the tendency of species to retain their climatic niches over evolutionary time 7 8 It is now also clear that part of this richness has been gained by the migration of lineages from other biogeographic regions 6 For instance pantropically distributed plant families such as Malpighiaceae Fabaceae and Annonaceae 6 9 10 11 originated at temperate latitudes as part of the former boreotropical flora 12 14 and subsequently entered the Neotropics via the mountain ranges of Central America and the newly formed Northern Andes One point in common to these hypotheses is the key role that the formation of the tropical Andes would have played in the www pnas org cgi doi 10 1073 pnas 0811421106 historical diversification of the Neotropical flora 15 Recent phylogenetic studies have shown that the Andean uplift acted both as a dispersal route for boreotropical lineages 16 17 and as a driver in promoting rapid diversification via allopatric speciation and ecological displacement in highland 16 19 and montane 11 habitats Fewer studies however have documented the impact of the Andean uplift on the lowland Amazonian flora Clearly the uplift must have affected these taxa by forming a new biotic barrier and profoundly changing the hydrology and climate of the region 20 Furthermore previous biogeographic studies on Andean radiations have typically considered the Andean orogeny as a single time limited event usually in connection with the final Miocene to Pleistocene uplift of the Andes 11 19 This contrasts with geological reconstructions indicating that the uplift took place in discrete periods progressing from south to north and from west to east and affecting different regions at different times 2 3 21 22 Episodic marine incursions related to global sea level rises during the extensional tectonic phases that followed periods of major uplift had a dramatic impact in the drainage patterns of the region as evidenced by paleogeographic and paleontological evidence 1 2 23 28 These marine incursions have been discussed in relation to their role as a pathway in the evolutionary transition from marine to freshwater habitats of Neotropical fishes 24 29 but they could also have acted as barriers to dispersal or as vicariance events fragmenting the ranges of terrestrial animals and plants It seems surprising that despite increasingly detailed geological reconstructions 2 24 26 28 thus far no study has attempted to document the effect of these events on the evolution of the Neotropical flora Generally detailed reconstructions have been hampered by the lack of resolution in many Andean species rich clades 19 Current biogeographic methods require well resolved phylogenies and uncertainty in phylogenetic relationships makes it difficult to reconstruct the specific sequence of geological vicariance and speciation events Here we use an integration of phylogenetic biogeographic and molecular dating methods to reconstruct the evolutionary history of tribes Cinchoneae and Isertieae which together form one of the major clades of Neotropical Rubiaceae The distriAuthor contributions A A and I S designed research A A and C P performed research J A A N and I S contributed new reagents analytic tools A A J A A N and I S analyzed data and A A and I S wrote the paper The authors declare no conflict of interest This article is a PNAS Direct Submission B H T is a guest editor invited by
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