Revealing the Secrets of African Annonaceae Systematics, Evolution and Biogeography of the Syncarpous Genera Isolona and Monodora Thomas L.P. Couvreur Promotor: Prof.dr. Marc S.M. Sosef Hoogleraar Biosystematiek Wageningen Universiteit Co-promotoren: Dr. James E. Richardson Higher Scientific Officer, Tropical Botany Royal Botanic Garden, Edinburgh, United Kingdom Dr. Lars W. Chatrou Universitair Docent, leerstoelgroep Biosystematiek Wageningen Universiteit Promotiecommissie: Prof.dr.ir. Jaap Bakker (Wageningen Universiteit) Prof.dr. Erik F. Smets (Universiteit Leiden) Prof.dr. Paul J.M. Maas (Universiteit Utrecht) Prof.dr. David Johnson (Ohio Wesleyan University, Delaware, USA) Dit onderzoek is uitgevoerd binnen de onderzoekschool Biodiversiteit Revealing the Secrets of African Annonaceae Systematics, Evolution and Biogeography of the Syncarpous Genera Isolona and Monodora Thomas L.P. Couvreur Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof.dr. M.J. Kropff in het openbaar te verdedigen op maandag 21 april 2008 des namiddags te vier uur in de Aula Thomas L.P. Couvreur (2008) Revealing the Secrets of African Annonaceae: Systematics, Evolution and Biogeography of the Syncarpous Genera Isolona and Monodora PhD thesis Wageningen University, The Netherlands With references – with summaries in English and Dutch. ISBN 978-90-8504-924-1 to my parents Contents CHAPTER 1: General Introduction 1 CHAPTER 2: Substitution Rate Prior Influences Posterior Mapping of Discrete Morphological Characters: an Unconventional Remedy 15 CHAPTER 3: Evolution of Syncarpy and other Characters in African Annonaceae: a Posterior Mapping Approach 35 CHAPTER 4: Unraveling the Evolutionary Origins of the East African Rain Forest Tree Flora 59 CHAPTER 5: Pollen Morphology of a Monophyletic Clade of Five African Annonaceae Genera 75 CHAPTER 6: Monograph of Isolona and Monodora (Annonaceae) 105 CHAPTER 7: General Discussion 255 REFERENCES 263 APPENDICES 276 ABSTRACT 287 SAMENVATTING 289 ACKNOWLEDGEMENTS 291 CURRICULUM VITAE 294 Chapter 1 General Introduction “Biodiversity is our most valuable but least appreciated resource” Wilson, E.O., 1992 1 BIODIVERSITY The Unit: Species Biological diversity, or simply biodiversity, surrounds (and inhabits) each and every one of us. Mankind has depended and will always depend on biodiversity for his survival. In fact, mankind itself is part of earth’s biodiversity. Vital substances such as food, medicine or shelter are all primarily derived from the diversity of species occurring on our planet, and that is why Wilson (1992) refers to it as “our most valuable resource”. But what exactly is biodiversity? It is fairly simple to understand what biodiversity is as a whole : it represents all living organisms, a bit like a dictionary representing all known words for a language. The tricky question lies in the determination of what biodiversity is composed of? The United Nations Convention on Biological Diversity defines biodiversity as “the variability among living organisms from all sources […]. This includes diversity within species, between species and of ecosystems.” Thus, from this definition we may conclude that species play a crucial role in defining biodiversity. Indeed, a ‘species’ is the direct outcome of evolution and represents the fundamental unit in the vast field of biology, from molecular biology to ecology as well as in evolution (de Queiroz, 2005). But what is a species? Interestingly, there is yet no satisfactory definition of what constitutes a species (Hey, 2001; Hey, 2006), even though this question is viewed as the “oldest and most fundamental in biology” (Dobzhansky, 1935). Over the last decades, a great deal of time and ink has been spent on trying to solve this problem, not just by biologist but also by philosophers. There exist over 20 species definitions based on different biological properties (for a review see Mayden, 1997). For example, the biological species concept uses the idea of reproductive isolation (Mayr, 1940) while the ecological species concept emphasizes the occupation of a distinct ecological niche (Van Valen, 1976). Any of these definitions has advantages as well as drawbacks, or are simply inapplicable to a certain extent. It is likely that the species problem will never have a clear solution: "The fact is that species are hard to define for a variety of reasons related to the various ways they can be truly indistinct, and no criterion that presumes to delineate natural boundaries can overcome this." (Hey, 2006). The theory of evolution by natural selection presented by Darwin (1859) was mainly based on the observation that species do not represent fixed entities as previously thought, but evolve through time. This led Dobzhansky (1955, p. 183) to state that if anyone could actually 1 General Introduction provide a “universally applicable, static definition of species” it would shed serious doubt over the whole modern theory of evolution. Despite this problem, the term species is widely used among researchers in biology as if a general, but ill-definable, consensus had been reached. It is important to recognize the difficulty in defining the word species, and to accept that the concept of ‘species’ is more a working hypothesis than a real entity. As in most fields of biology, when the reality is too complicated to capture (be it a definition or a process) one has to clearly define the working hypotheses or assumptions used in a study. In a taxonomic revision this means explicitly stating the species concept used (Luckow, 1995). In this thesis we follow the phylogenetic species concept (Cracraft, 1983; Nixon and Wheeler, 1990) in that the hypothesis of a species is formulated by identifying the smallest aggregation of individuals diagnosable by a unique combination of constant (or fixed) character states observable by ordinary morphological means (Snow, 1997). “Ordinary morphological means” refers to morphological characters that are immediately visible on the herbarium sheets or require no more that 30x magnification (e.g. hairs). The consistency of character states across individuals of the same species is interpreted as reliable and indicative of the existence of a common history shared among them (Luckow, 1995; Snow, 1997). In addition, we do not consider a species to be polyphyletic, i.e. a group of individuals with several different most recent common ancestors. The Tool: Systematics Putting the debate of ‘what are species’ aside, it is generally accepted that the fundamental unit of biodiversity is the species (Claridge et al., 1997). Estimates of the Earth’s total number of species varies greatly, from 4 to 100 million species (Pennisi, 2003), but 14 million is a widely accepted number. The fact that we cannot provide a better estimate underlines how little we know about what builds up biodiversity. Identifying, describing, classifying and naming Earth’s biodiversity as well as understanding the evolutionary relationships between species is the major role of the branch of biology called “systematics” or “taxonomy” 1. Systematics is one of the oldest scientific disciplines and every culture has developed some kind of system to classify the plants and animals they encounter and use. How much have we already described? Well, not much. Estimates vary once again, ranging from 1.4 to 1.7 million described species (Pennisi, 2003). Thus much work is still needed. Unfortunately, our time is limited. In the past decades the use of the term “biodiversity crisis” has been on the increase in the media. In the coming decades we shall see a major loss of species diversity, almost completely caused by human actives. We are still far from 1 There appears to be some confusion between the words taxonomy and systematics (De Queiroz, 1988). Some consider them as two separate entities, with systematics concerned with the study of relationships between living organisms and taxonomy with the identification and classification of species into a scheme of words (e.g. Wiley, 1981). Others suggest that taxonomy encloses systematics and classification (De Queiroz, 1988). In this thesis I use the term systematics to refer to the action of describing the species as well as studying their evolutionary relationships. 2 Chapter 1 inventorying and understanding the world’s biodiversity and yet it is already disappearing at a quick and steady pace. There are three good reasons why the loss of biodiversity and the ecosystems in which they occur in should not be ignored. First, the undescribed but disappearing biodiversity could provide valuable resources yet to be exploited. We have gained so much already from the meager ca. 12% 2 of described biodiversity, who knows what we can find in the rest. Second, some species occupy a more important role in a particular ecosystem than others. Such species are called “keystone” species (Mills et al., 1993). The basic idea is that if a keystone species goes extinct or disappears from the ecosystem this will have repercussions on many other species that depend on it (e.g. an animal species that disperses the seeds of numerous different tree species). Thus the loss of even a fairly low number of species could lead to the collapse of entire ecosystems because of these close interrelationships and existing interdependences of species. Finally, the loss of species and their ecosystems will lead to the loss of the evolutionary potential from which this diversity is generated. Loss of entire ecosystems will