Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2013 South American Cacti in time and space: studies on the diversification of the tribe Cereeae, with particular focus on subtribe Trichocereinae (Cactaceae) Lendel, Anita Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-93287 Dissertation Published Version Originally published at: Lendel, Anita. South American Cacti in time and space: studies on the diversification of the tribe Cereeae, with particular focus on subtribe Trichocereinae (Cactaceae). 2013, University of Zurich, Faculty of Science. South American Cacti in Time and Space: Studies on the Diversification of the Tribe Cereeae, with Particular Focus on Subtribe Trichocereinae (Cactaceae) _________________________________________________________________________________ Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr.sc.nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Anita Lendel aus Kroatien Promotionskomitee: Prof. Dr. H. Peter Linder (Vorsitz) PD. Dr. Reto Nyffeler Prof. Dr. Elena Conti Zürich, 2013 Table of Contents Acknowledgments 1 Introduction 3 Chapter 1. Phylogenetics and taxonomy of the tribe Cereeae s.l., with particular focus 15 on the subtribe Trichocereinae (Cactaceae – Cactoideae) Chapter 2. Floral evolution in the South American tribe Cereeae s.l. (Cactaceae: 53 Cactoideae): Pollination syndromes in a comparative phylogenetic context Chapter 3. Contemporaneous and recent radiations of the world’s major succulent 86 plant lineages Chapter 4. Tackling the molecular dating paradox: underestimated pitfalls and best 121 strategies when fossils are scarce Outlook and Future Research 207 Curriculum Vitae 209 Summary 211 Zusammenfassung 213 Acknowledgments I really believe that no one can go through the process of doing a PhD and come out without being changed at a very profound level. Not necessarily because of the PhD itself but because of the surroundings, circumstances, pressure, doubts, questioning and reflections one experiences during that process. The same stands for me. Being away from home for the very first time I learned a lot; about the world but mostly about myself. I’ve visited beautiful places, met some extraordinary people, widened my personal limits and found the strength I never knew I had in me. And none of this would be possible without many people that deserve to be mentioned here. One person that stands out is Merran Matthews who was a constant perpetuator for me during this process. She found most unorthodox ways to encourage me and “keep me in the game” for which I stay deeply grateful to her. Aelys Humphreys was there for me to discuss within deepest details various thematic overwhelming me at the time – from family values to simplifying approaches I took in a particular project. I profited a lot from conversations with her and thank her for that. Certainly this PhD would never see the light of the day without being supervised by experienced and competent people like Reto Nyffeler, Peter Linder and Urs Eggli. I thank Reto for taking me along this journey and not giving up on me, Peter for supporting this project and me as a person and Urs for generously sharing his knowledge on cacti. Alexandre Antonelli was a “distant player” who would occasionally, still just when needed, bring in an idea or put things into perspective - and that would fuel me to keep on going. Elena Conti was always happy to share her experiences, connected either to science or family issues and I thank her for that. Expert in a floral morphology and with a profound knowledge of angiosperm fossils, Peter Endress was always happy to share his knowledge and together with Merran has provided multiple occasions for me to work on their projects, helping me to stay in Switzerland, financially sustain my thesis and learn valuable techniques, that in many days felt like much needed meditation. Niklaus Müller was always happy to help when my limited knowledge in informatics did not allowed me to continue and I have a feeling that Alex Bernhard was more than amused with my questions on Adobe Illustrator. Dirk Karger is thanked for translating thesis summary to German. I was lucky enough to discuss methods, techniques and approaches with people that I got to know in the Institute of Systematic Botany: Timo Van der Niet, Jurriaan de Vos, Chloé Galley and Mike Pirie are thanked for their patience while willing to teach and help me with stubborn programs - in many occasions. Marlon Machado was the person who opened up the world of cacti to me. By taking me to meetings of the cactus and succulent societies he made me discover how many people are passionate by this group of plants. It made a great impression on me to see and to meet in person members of the public, non-scientists who actually read our papers and base their knowledge about cacti on our findings – a kind of last stop in a world of science, but unfortunately a stop that many scientists never manage to meet or somehow forget exists. Cyril Guibert was kind enough to travel with me to 1 California and I thank him for taking the wheel through Los Angeles. I shared in many occasions the load of being a PhD student with Cécile Allanic, Ljiljana Krstin, Lukas Taxböck, Catarina Rydin, Jason Grant and Claire Arnold, and I thank them for listening and encouraging me to continue. Coming to work seemed somehow easier knowing that Gabriele Salvo, Julien Bachelier and Serge Haemmerli will be working next to me and depending on the need will be ready to help, share, or laugh with me. With many of the above mentioned people I shared more than only work - together we partied, laughed and cried. With some of them I stayed in contact, with others less, but regardless I consider them to be my dearest friends, with whom I shared a part of my life and if and whenever our life paths cross again they will never be strangers for me. And last but not the least the people without whom this PhD would never be completed, and to whom I am indebt the most, are my family. Thank you Pascal for supporting me on this long and painful journey. Thank you Isabelle for being my daughter. My parents, Marica and Mijo together with my brother Dragan Lenđel were more than great in believing in me and giving me opportunities to work by taking care of Isabelle. For this task also many neighbors and friends jumped in and for it I thank Vania Widmer, Jacques Rueger, Chloé Tornay, Andreas Sonderegger, Caroline Barras, and Isabelle Chablais. Family Burkitt is thanked for providing a cosy place to stay at, during the days (nights) before submitting the thesis. 2 Introduction Cacti are among the most conspicuous and characteristic plants of arid and semiarid areas in the New World. The family Cactaceae is remarkable for its great diversity of specialized growth form characteristics, floral morphology, and pollination syndromes. The scientific study of Cactaceae, consisting of about 130 genera and 1850 species (Nyffeler and Eggli 2010b) has long been neglected, in spite of many fascinating aspects concerning their evolutionary biology. Even though there are numerous cactus books dedicated to amateurs, the number of detailed taxonomic studies of genera and species groups are very limited (e.g. Leuenberger 1986, Taylor 1991, Zappi 1994, Leuenberger 1997, Nyffeler 1998). The number of names, in most cases not adequately typified, exceeds more than 10 times the number of supposedly „acceptable“ entities and makes the work for monographs very cumbersome (e.g., Hunt 1991). During the past, a wide range of contrasting conceptions took turns, either preferring a more conservative and lumper’s approach or arguing for a splitters approach. This fact can be explained by the difficulties to arrive at a sound biological classification system by using morphological characters. Furthermore, a lack of thorough phylogenetic studies prevented so far to resolve controversial opinions on relationships and classification. Overall, a small number of molecular phylogenetic studies have been devoted to Cactaceae up to now, resolving phylogenetic relationships between cacti and its closest relatives (Nyffeler 2007, Nyffeler and Eggli 2010a), among major clades within the cactus family (Nyffeler 2002, Ocampo and Columbus 2010, Bárcenas, et al. 2011, Hernández- Hernández, et al. 2011), at the base of the cactus phylogeny (Butterworth and Wallace 2005, Edwards, et al. 2005, Butterworth and Edwards 2008), as well as among various suprageneric and generic groups of Cactoideae and Opuntioideae (e.g., Demaio, et al. 2011, Mosti, et al. 2011, Schlumpberger and Renner 2012). The typical cactus growth form, characterized by the absence of leaves, stems that stay green and photosynthetically active for several seasons, spine clusters associated with side branches, and a reduced branching pattern is also found in other, unrelated groups of eudicot plant families (i.e., Apocynaceae, Euphorbiaceae). It represents one of the classical textbook example for “convergent evolution” for adaption to a prominent ecological factor (i.e., temporal aridity; Niklas 1997, Futuyma 1998). The traditional idea put forward by Buxbaum (1956) in his „law of the abbreviation of the vegetative phase” is that there is a general „trend“ in cactus evolution leading from branched, arborescent-columnar forms to unbranched, solitary, globular types (e.g. Buchheim 1964, Cullman, et al. 1984, see Nyffeler and Eggli 2010b). This idea concerning cactus evolution (Fig.1) and relationships is still widely prevailing and is reflected in current classification systems ( e.g. Buchmann 1964, Cullmann, et al. 1984) . 3 Figure 1. Schema of the prevailing concept on cactus evolution, showing reduction of the vegetative phase. However, recent molecular systematic analyses (e.g., Fig. 2; Hernández-Hernández, et al. 2011, Schlumpberger and Renner 2012) documented evidence that these ideas concerning the pattern of growth form evolution in cacti need to be revised (see also Griffith 2004a, Griffith 2004b).