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Tracing the Evolutionary History of Coca (Erythroxylum)

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Tracing the Evolutionary History of Coca (Erythroxylum) TRACING THE EVOLUTIONARY HISTORY OF COCA (ERYTHROXYLUM) by MELISSA ISLAM B.S, Colorado State University, 1997 M.S., Colorado State University, 2005 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology & Evolutionary Biology 2011 This thesis entitled: Tracing the Evolutionary History of Coca (Erythroxylum) written by Melissa Islam has been approved for the Department of Ecology & Evolutionary Biology Tom A. Ranker, Chair Susan Beatty Pam K. Diggle Robert P. Guralnick Andrew P. Martin Date: May 2, 2011 The final copy of this thesis has been examined by the signatories, and we Find that both the content and the form meet acceptable presentation standards Of scholarly work in the above mentioned discipline. Islam, Melissa (Ph.D., Ecology & Evolutionary Biology) Tracing the Evolutionary History of Coca (Erythroxylum) Thesis directed by Professor Tom. A. Ranker Abstract The tropical, flowering shrubs in the genus Erythroxylum (230 species) are commonly known as coca. For 8,000 years, two Erythroxylum species have been exploited for their production of cocaine. Coca plants remain culturally significant and economically important. Yet, their origin and evolutionary history, especially of the cultivated species, have not been explored in a modern phylogenetic framework. Molecular and morphological characters were used to reconstruct the evolutionary history of the genus to determine the intrageneric relationships within Erythroxylum and origin of cocaine synthesis, to infer the evolutionary history of the cultivated species and the number of domestication events, and to determine the origin and diversification of the Caribbean Erythroxylum. Distribution of Erythroxylum across the tropics resembles a Northern Tropical Gondwanan distribution resulting from the break-up of Gondwana. The age of divergence of Erythroxylum along with the hypothesized origin of the South American species supports a boreotropical dispersal rather than a Gondwanan origin. Eighty years ago, the genus was split into 19 sections based on a few morphological characters. Many of these sections are heterogeneous and likely not predictive of evolutionary relationships. Testing the monophyly of these sections revealed only one monophyletic section. Strongly supported clades were given informal names with at least one morphological feature identified that is shared by the members of each clade. Multiple origins of cocaine synthesis were inferred. For the cultivated species, E. novogranatense, was hypothesized to be derived through human selection from E. coca. These two species were supported as distinct species indicating at least two domestication events of wild Erythroxylum species. Their closest wild relatives are section Archerythroxylum species with deciduous leaves. The Caribbean Erythroxylum species arose from multiple colonization events, including three long- distance dispersal events from northern South America and one from Mexico or Central America. Species from the same island were not monophyletic indicating species on the same island originated independently from either other islands or continental species, except for a large Cuban and Hispañiolan clade. This clade indicates a radiation within Cuba with one or two dispersal events to Hispañiola. Updated taxonomy and occurrence of the Caribbean species is reviewed. iii Table of Contents CHAPTER ONE: Phylogeny and systematics of Erythroxylum (Erythroxylaceae) and the origin of cocaine synthesis ........................................................................................................................................... 1 Introduction ............................................................................................................................................... 1 Materials and Methods .............................................................................................................................. 2 Plant material. ...................................................................................................................................... 2 Morphological characters. ................................................................................................................... 4 Molecular characters. ........................................................................................................................... 6 Data analyses. ....................................................................................................................................... 8 Results ..................................................................................................................................................... 10 Discussion ............................................................................................................................................... 17 Erythroxylaceae systematics. .............................................................................................................. 17 Monophyly of Erythroxylum. .............................................................................................................. 19 Schulz’s Sections. ................................................................................................................................ 20 Origin of cocaine synthesis. ................................................................................................................ 26 Summary. ............................................................................................................................................ 29 CHAPTER TWO: The Evolutionary History of the Cultivated Cocas (Erythroxylum) ............................. 32 Introduction ............................................................................................................................................. 32 Materials and Methods ............................................................................................................................ 33 Plant material. .................................................................................................................................... 33 Morphological characters. ................................................................................................................. 36 Molecular characters. ......................................................................................................................... 36 Data analyses. ..................................................................................................................................... 37 Results ..................................................................................................................................................... 39 Discussion ............................................................................................................................................... 45 Wider context. ..................................................................................................................................... 46 Relationships among the cultivated cocas. ......................................................................................... 46 Monophyly of cultivated cocas. ........................................................................................................... 48 Origin and wild relatives. ................................................................................................................... 49 Summary. ............................................................................................................................................ 51 CHAPTER THREE: Phylogeography of Caribbean Erythroxylum ............................................................ 53 Introduction ............................................................................................................................................. 53 Materials and Methods ............................................................................................................................ 58 Plant material. .................................................................................................................................... 58 Morphological characters. ................................................................................................................. 59 Molecular characters. ......................................................................................................................... 59 Data analyses. ..................................................................................................................................... 60 Results ..................................................................................................................................................... 63 Discussion ............................................................................................................................................... 67 Number of colonization events. ........................................................................................................... 69 Origin of Caribbean Erythroxylum. .................................................................................................... 69 Relationships among Caribbean Erythroxylum. ................................................................................. 71 Summary. ...........................................................................................................................................
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