University of Gothenburg Faculty of Science 2008 SPATIOTEMPORAL EVOLUTION OF NEOTROPICAL ORGANISMS NEW INSIGHTS INTO AN OLD RIDDLE Alexandre Antonelli Doctoral Thesis This thesis will be defended in public at 10.00 A.M. on November 28th, 2008 in the Lecture Hall, Department of Plant and Environmental Sci- ences, Carl Skottsbergs Gata 22B, Göteborg, Sweden. Faculty opponent: Prof. Mari Källersjö Examiner: Prof. Nils Hallenberg © Alexandre Antonelli, 2008. All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, without written permission. Antonelli, A. 2008. Spatiotemporal Evolution of Neotropical Organ- isms: New Insights into an Old Riddle. Doctoral Thesis. Department of Plant and Environmental Sciences, University of Gothenburg, Göte- borg, Sweden. Cover image: “Romantic view over Nebo”, by Karl Axel Pehrson (1921–2005), Swedish artist and creator of the statuette for the Swedish Film Award Guldbaggen, The Golden Beetle. As in all his paintings, the landscape and organisms portrayed are purely imaginary. Courtesy: County Museum of Örebro, Sweden. ISBN: 978-91-85529-21-6 http://hdl.handle.net/2077/17695 Printed by Geson Hylte Tryck. 2 To Anna 3 4 Contents Abstract ................................................................................................... 6 List of original papers ............................................................................. 7 Introduction ............................................................................................. 8 The Neotropical region ...................................................................... 8 Neotropical biodiversity ................................................................... 10 Distributional patterns ...................................................................... 13 Models of diversification ................................................................. 15 Objectives ............................................................................................. 18 Material and methods ............................................................................ 19 Study groups .................................................................................... 19 Sequence regions .............................................................................. 22 Phylogenetic inference ..................................................................... 24 Age estimations ................................................................................ 25 Analyses of extinction ...................................................................... 26 Biogeographic reconstruction .......................................................... 26 Results and Discussion ......................................................................... 30 Phylogenetic and taxonomic implications ........................................ 30 Time and mode of diversification .................................................... 33 Methodological considerations ........................................................ 51 Conclusions ........................................................................................... 53 Abbreviations and time scale ................................................................ 55 References ............................................................................................. 56 Svensk populärvetenskaplig sammanfattning ....................................... 70 Resumen en Español ............................................................................. 76 Acknowledgements ............................................................................... 79 5 Abstract owhere else on Earth are there so many species of plants and animals as in the Neotropical region. Yet, many questions re- Nmain concerning the causes underlying such outstanding diver- sification. In this thesis, I use a combination of molecular-based methods (phy- logenetic inference, molecular dating, biogeographic reconstruction, analyses of diversification and extinction) together with geological, palaeontological, hydrological and climatological evidence to recon- struct the evolution of some Neotropical organisms in space and time. Diversification patterns obtained from case studies in the plant families Rubiaceae, Chloranthaceae and Campanulaceae are compared to pub- lished studies of other plants and animals, especially tetrapods (birds, non-avian reptiles, amphibians and mammals). The uplift of the Northern Andes in the Neogene (~23 Ma to today) is concluded to have played a major role in promoting Neotropical di- versification, by fostering allopatric speciation of lowland organisms and inducing adaptive radiations in newly formed montane habitats. In addition, its formation caused the end of a lowland corridor episodically invaded by marine incursions that separated the Northern and Central Andes, enabling the southward dispersal of boreotropical groups al- ready present in northwestern South America. The fact that most Neotropical plant groups are either Andean- centred or Amazonian-centred is explained by the long-lasting effect of the Palaeo-Orinoco and Lake Pebas as dispersal barriers between these two diversity centres. Finally, a new diversification model is proposed to explain the origin and evolution of organisms in two areas character- ized today by unusually high levels of species richness and endemism: the Huancabamba region and western Amazonia. Under this model, speciation is proposed to have occurred over several million years in connection with the recolonization of previously submerged areas, by means of adaptive radiation of founder colonies and secondary contact of previously isolated populations. KEYWORDS: Neotropics; Biodiversity patterns, Speciation models, Andean uplift, K/T Event; Biogeography, Phylogenetics, Molecular dating; Rubiaceae, Chloranthaceae, Campanulaceae, Tetrapods. 6 List of original papers This thesis is based on the following papers. They will be referred to in the text by their Roman numerals. I. Andersson, L., Antonelli, A. (2005) Phylogeny of the tribe Cin- choneae (Rubiaceae), its position in Cinchonoideae, and descrip- tion of a new genus, Ciliosemina. Taxon 54 (1):17–28. II. Antonelli, A. (2008) Higher level phylogeny and evolutionary trends in Campanulaceae subfam. Lobelioideae: Molecular signal overshadows morphology. Molecular Phylogenetics and Evolution 46 (1):1–18. III. Antonelli, A., Quijada-Masareñas, A., Crawford, A.J., Bates, J.M., Velazco, P.M., Wüster, W. (accepted) Molecular studies and phylogeography of Amazonian tetrapods and their relation to geo- logical and climatic models. In: Hoorn, C., Vonhof, H., Wessel- ingh, F.: Amazonia, Landscape and Species Evolution: a Look into the Past. Blackwell publishing. IV. Antonelli, A., Nylander, J.A.A., Persson, C., Sanmartín, I. (sub- mitted) Tracing the impact of the Andean uplift on Neotropical plant evolution: evidence from the coffee family. V. Antonelli, A., Sanmartín, I. (submitted) Reconstructing the spatio- temporal evolution of the ancient angiosperm genus Hedyosmum (Chloranthaceae) using empirical and simulated approaches. VI. Antonelli, A. (submitted) Convergence not always the case. Papers I and II reprinted with permission. 7 Introduction “In England any person fond of natural history enjoys in his walks a great advantage, by always having something to attract his attention; but in these fertile lands teeming with life, the attractions are so numer- ous, that he is scarcely able to walk at all.” Charles R. Darwin, 19th April 1939, during his stay in Brazil. The Neotropical region The word Neotropic (from the Greek neos = “new”) refers to the tropi- cal region of the American continent, or “New World” – a term coined by Peter Martyr d’Anghiera in 1493 shortly after Christopher Colum- bus’ first voyage to the Americas (O'Gorman 1972). As currently de- fined (Schultz 2005), the Neotropic ecozone extends from central Mex- ico in the north to southern Brazil in the south, i.e. including Central America, the Caribbean islands and most of South America. Geologically, the Neotropics are distributed across three tectonic plates: the North American, the Caribbean and the South American (Fig. 1), each with a very different geological history. The South American and African plates remained fused in the giant palaeoconti- nent of Gondwana for hundreds of millions of years until its final break- up about 100 million years ago (Ma; Scotese 2001). The fact that most tropical soils are extremely scarce of nutrients reveals long-lasting weathering conditions. 8 NEO- TROPICS Figure 1. The Neotropical region extends from central Mexico in the north to southern Brazil in the south, thus occupying the North American, the Carib- bean and the South American tectonic plates. Many hypotheses of diversifica- tion discussed in this thesis derive ultimately from the geological dynamics of these plates: the separation of Africa and South America, the rise of the Andes and the reconnection of South America with a land mass after 90 million years of isolation. (Source: Wikimedia Commons). Precipitation and annual mean temperatures are generally high, but there is great regional variation. Whereas some places in South America have amongst the highest precipitation rates in the world (such as Quibdo in western Colombia, with almost 9000 mm annually), other regions are extremely dry. Perhaps surprisingly, it is in South America that the driest place on Earth is to be found: Calama, in the subtropical