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The Uses of Molecular Dating Analyses in Evolutionary Studies, with Examples from the Angiosperms Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Frank Kaspar Rutschmann von Zürich ZH Promotionskomitee: Prof. Dr. Elena Conti (Vorsitz) Prof. Dr. Peter Linder Dr. Torsten Eriksson Zürich 2006 Acknowledgements First of all, I would like to express my gratitude towards my supervisor, Elena Conti. The last four years would not have been as exciting and fruitful without your full support. I really appreciate your style of supervision which gave me the freedom to explore the things I was fascinated about. I am very impressed by your enthusiasm and your dedication to all sorts of biological questions, but especially by your social empathy. Your office door was always open for all kinds of questions - even beyond biology. I would also like to thank Peter Linder - it was a great pleasure to collaborate with you, and your sense of humor made the struggle with statistics and manuscripts much more fun. A great deal of laughter was also initiated by my fantastic and very patient office mates Merran Matthews, Josephine Jacksch and Gabriele Salvo, who often supplied me with mental and physical calories. But also Timo van der Niet, Sandro Wagen, Zsófia Hock and Péter Szövényi, Evelin Pfeifer, Urs Landergott, Brigitte Marazzi, Claudia Winteler, Chloé Galley, Rolf Rutishauser, Niklaus Müller, Alex Bernhard, Jakob Schneller, Burgi Liebst, Melanie Ranft, Rosemarie Sigrist, Reto Nyffeler, Daniel Heinzmann, Jürg Schönenberger, Maria von Balthazar, and many other members of the institute contributed to an enjoyable atmosphere and many cheerful discussions. The staff of the secretariat, the library, and the botanical garden made every journey outside the office a pleasure and provided an efficient working environment, especially Corinne Burlet, Claudio Brun, Barbara Seitz, Elena Benetti, Nadine Kofmehl, Elisabeth Schneeberger, and Daniel Schlagenhauf. Finally, I would like to thank my family and friends, who supported me in many different ways. Thank you so much, Corinne Furrer, Anne and Christian Rutschmann, Dieter Rutschmann, Annette and Jochen Wild, Andri Schläpfer and Linda Zehnder, Renata and Hansjörg Schlaepfer, Philip Moline and Saskia Lampert, Nikolaus Amrhein, Annemarie and Niklaus Kohler-Pfister, Frances Athanasiou, Torsten Eriksson, Stephan Lange, Karen Hilzinger, Christoph Eichenberger, Beat Seiler, Lilo Michel, Lukas and Thomas Furrer, Dominique Sirena, Corsin Müller, Florian Steiner, and Jonas Wittwer. Last but not least I owe much to my parents who have supported me in all conceivable ways. I can sincerely say that without you, this project would not have been possible. I therefore would like to dedicate this work to my mother, Margrit Rutschmann, and my late father, Peter Rutschmann. Table of Contents Publication list ......................................................................................................... 4 General introduction ............................................................................................. 5 Chapters: I. Molecular dating of phylogenetic trees: A brief review of current methods that estimate divergence times .................... 13 II. Did Crypteroniaceae really disperse out-of-India? Molecular dating evidence from rbcL , ndh F, and rpl 16 intron sequences ........ 47 III . Calibration of molecular clocks and the biogeographic history of Crypteroniaceae: A reply to Moyle ............................................................... 85 IV . Tempo and mode of diversification in the African Penaeaceae and related taxa .................................................................................................. 93 V. Assessing calibration uncertainty in molecular dating: The assignment of fossils to alternative calibration points .............................. 137 VI. Taxon sampling effects in molecular clock dating: An example from the African Restionaceae .................................................... 187 General summary .............................................................................................. 219 Zusammenfassung ............................................................................................ 221 Lebenslauf ............................................................................................................ 225 Publication list The following publications stem from my years as a Ph.D. student at the Institute of Systematic Botany, University of Zurich, Switzerland (2002-2006). They represent ten articles, of which I have written five as a first or single author. Four papers are already published. The most recent work is listed first. Rutschmann, F., J. Schönenberger, H.P. Linder, and E. Conti. Tempo and mode of diversification in the African Penaeaceae and related taxa. In preparation. Barker N.P., P.H. Weston, and F. Rutschmann. Molecular dating of the radiation of the Proteaceae is only partially congruent with the breakup of Gondwana. In preparation. Rutschmann F., T. Eriksson, K. Abu Salim, and E. Conti. Assessing calibration uncertainty in molecular dating: The assignment of fossils to alternative calibration points. Submitted to Systematic Biology. Schlaepfer H. and F. Rutschmann. Deriving species responses from vegetation relevés: an iterative approach. Submitted to Botanica Helvetica . Schönenberger, J., E. Conti, F. Rutschmann, and R. Dahlgren. Penaeaceae in K. Kubitzki, ed. The families and genera of vascular plants. Vol. 9. Springer, Berlin. In press. Rutschmann F. 2006. Molecular dating of phylogenetic trees: A brief review of current methods that estimate divergence times. Diversity and Distributions 12 : 35-48. Linder H.P., C. R. Hardy, and F. Rutschmann. 2005. Taxon sampling effects in molecular clock dating: An example from the African Restionaceae. Molecular Phylogenetics and Evolution 35 : 569–582. Conti E., F. Rutschmann, T. Eriksson, K. Sytsma, and D. Baum. 2004. Calibration of molecular clocks and the biogeographic history of Crypteroniaceae: A reply to Robert G. Moyle. Evolution 58 (8): 1874-1876. Rutschmann F. 2005. Bayesian molecular dating using PAML/multidivtime. A step-by-step manual, version 1.5 (July 2005). University of Zurich, Switzerland. Available at http://www.plant.ch . Rutschmann F., T. Eriksson, J. Schönenberger, and E. Conti. 2004. Did Crypteroniaceae really disperse out-of-India? Molecular dating evidence from rbc L, ndh F, and rpl 16 intron sequences. International Journal of Plant Sciences 165 (4 Suppl.): 69-83. 4 General introduction In the quest of understanding evolutionary mechanisms and processes, accurate information about the timing of specific events in the past is needed. For example, it is important to know how fast retroviruses like the human immunodeficiency virus (HIV) change their genotype, in order to design new drugs or vaccines that will work also for future strains (Korber et al. , 2000). Or, to mention another fascinating example, it is of general interest - even beyond the life sciences - to know when the first humans started to diverge from the chimpanzees (between 6.3 and 5.4 million years ago; Patterson et al. , 2006). Until forty years ago, information about the timing of past evolutionary events was only available in the form of fossils. Fossils are usually dated based on age estimates of the stratigraphic layer in which they are found, and they can be assigned to modern taxa by comparing the morphological characters preserved in the fossil with the traits of extant species (Hennig, 1969; Doyle and Donoghue, 1993). However, most organisms that once populated our planet have not been preserved in the fossil record, or their fossils have not been detected so far (Darwin, 1859). This implies that for most organisms, no direct information about their phylogenetic age is available. In 1965, Zuckerkandl and Pauling postulated that the amount of difference between the DNA molecules of two species is a function of the time since their evolutionary separation. This was shown by comparing protein sequences (hemoglobins) from different species and further comparing amino acid substitution rates with ages estimated from fossils. Based on these early findings, standard techniques were developed to infer time information from molecular (DNA or protein) distances among species, giving origin, over time, to a range of different molecular dating methods (Magallón, 2004; Welch and Bromham, 2005; Penny, 2005). In general, a molecular dating study begins with the reconstruction of the phylogenetic relationships among selected taxa. Then, specialized dating methods are used to transform the phylogenetic tree into an ultrametric tree. Whereas branch lengths in the phylogram represent the number of absolute molecular substitutions, they express relative time of lineage persistence in the ultrametric tree. The transformation of relative into absolute time requires some type of calibration, for which external time information – either stemming from fossils or from dated paleogeologic events - is assigned to at least one node of the phylogeny (Sanderson, 1998). The results of such a molecular dating analysis are estimates of divergence times for every lineage, summarized in a chronogram. 5 Under the assumption of a strict molecular clock, all branches of a phylogenetic tree evolve at the same, global substitution rate, which makes the second step, the reconstruction of an ultrametric
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