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Origins of Diversity: the Evolutionary Genetics of Caribbean Butterflies

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Origins of Diversity: the Evolutionary Genetics of Caribbean Butterflies ORIGINS OF DIVERSITY: THE EVOLUTIONARY GENETICS OF CARIBBEAN BUTTERFLIES. A thesis submitted in fiilfilment of the requirements for the degree of Doctor of Philosophy by Neil Davies London, July 1995 ProQuest Number: 10055864 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest. ProQuest 10055864 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 I do not know wiiat I may appear to the world, but to myself I seem to have been only like a boy playing on the seashore, and diverting myself in now and then finding a smoother pebble or a prettier shell than ordinary, whilst the great ocean of truth lay all undiscovered before me. Isaac Newton TO MY PARENTS TABLE OF CONTENTS A bstract 6 Acknowledgements 8 1. Introduction 10 1.1. Bibliography 14 2. The species richness of West Indian butterfly faunas 2.1. Abstract 16 2.2. Introduction 17 2.3. Methods 21 2.4. Results 29 2.5. Discussion 34 2.6. Bibliography 52 2.7. Tables 66 2.8. Figures 70 3. Genetic differentiation in four species of West Indian butterfly 3.1. Abstract 74 3.2. Introduction 75 3.3. Methods 80 3.4. Results 84 3.5. Discussion 89 3.6. Bibhography 100 3.7. Tables 107 3.8. Figures 111 3.9. Appendices 120 4. The historical biogeography of the West Indian butterfly Dtyas iulia (Lepidoptera: Heliconiidae) 4.1. Abstract 134 4.2. Introduction 135 4.3. Methods 137 4.4. Results 140 4.5. Discussion 142 4.6. Bibliography 146 4.7. Tables 150 4.8. Figures 152 5. The island biogeography of genetic variation 5.1. Abstract 156 5.2. Introduction 157 5.3. Methods 160 5.4. Results 162 5.5. Discussion 164 5.6. Bibhography 174 5.7. Tables 178 5.8. Figures 179 6. Classifying island populations 6.1. Abstract 187 6.2. Bibhography 196 7. Fuzzy species 7.1. Abstract 200 7.2. Bibhography 217 7.3. Figures 222 8. Reproductive isolation in a butterfly hybrid zone: a subtle Haldane effect 8.1. Abstract 224 8.2. Introduction 225 8.3. Methods 227 8.4. Results 233 8.5. Discussion 237 8.6. Bibhography 242 8.7. Tables 246 9. Haldane’s rule: old theories are the best 9.1. Introduction 258 9.2. Bibhography 264 9.3. Figure 266 ABSTRACT Darwinian evolution requires and generates biodiversity. The biodiversity of West Indian butterflies is investigated at the population and species level The latest butterfly species numbers for West Indian islands are presented and the fectors wdiich influence community richness are determined. Area is by far the most significant physical variable. The nature of the species-area relationship is affected by community size: smaller communities seem more vagile, flattening the species- area curve. The genetic structure of four West Indian butterflies is surveyed using allozyme electrophoresis. A phenotypic tendency towards subspeciation is corroborated by the allozyme data. A long-standing controversy in West Indian biogeography is whether the 6una arose by dispersal from the continent, or is the remnants of a continental fruna isolated by ancient geological events. Whilst the action of vicariance cannot be conq)letely ruled out, any lasting inq)ression has certainly been masked by more recent dispersal. One of the species, Dryas iulia, has a particularly complex genetic structure in the West Indies. A survey of mtDNA variation confirms the major phylogenetic breaks identified by the allozyme data. Apphcation of the molecular clock indicates a major separation between West Indian Dryas iulia and continental populations around 2.5 million years ago. This is too recent for the vicariance hypothesis. Classification is inevitably difficult with insular populations, some of which are on the borderline between differentiated subpopulation and separate species. Such populations, although anticipated by evolutionary biology, represent a challenge for taxonomy. The difficulties are discussed with particular reference to phylogeny reconstruction. The species-subspecies interface is also examined empirically. Pre and postzygotic isolation between two hybridising Central American butterflies are evaluated. The results are discussed in the context of spéciation genetics, particularly Haldane’s rule. Muller’s dominance theory is assessed as an explanation for Haldane’s rule. ACKNOWLEDGEMENTS Many people have contributed to this project and the following deserve special thanks. My supervisor, Andrew Pomiankowski, allowed me the freedom to leam from my own mistakes whilst making sure I didn’t stray too far off track. Ifis comments and criticisms, along with those of Jim Mallet, have added greatly to this thesis. Much of my time was spent with the University of Puerto Rico (UPR) at Mayaguez and the Smithsonian Tropical Research Institute (STRI) in Panama. I am very grateful to both institutions for their support. In particular I would like to thank Stuart Ramos of the UPR for providing space in his laboratory and sharing his great knowledge of West Indian butterflies. Annette Aiello and Eldredge Bermingham, from STRI, provided invaluable advise and assistance, for which I will always be grateful. Collecting specimens was made more pleasurable and productive thanks to numerous people, only a few of which are mentioned here: Luis Roberto Hernandez, Jesus Bretado and Behsario Cepeda, Lee and Jaquie Miller, Tom Turner, Kelvin Antonio, Dennis Knowles, Peter Evans, Grilles Seutin, Adela Olivardia, and Messrs. Bonnet, Fennec and Tanasi. I would also like to thank Igor Emelianov, Peter King, Owen McMillan and Stephen Stokes. This project would never have happened had it not been for David Spencer Smith, who introduced me to West Indian butterflies. He has continued to play an important and valued role in my studies. I thank him, and his wife Sylvia, for their he^ and friendship over the past four years. Finally I have to thank my frmily - for everything really, but not least their tolerance during the writing of this thesis. Financial support was provided by a Science and Engineering Research Council Ph.D. studentship, a short-term fellowship from the Smithsonian Institution and a Galton bursaiy from the Department of Genetics and Biometry, University College London. CHAPTER 1 INTRODUCTION This project began with the 1989 Oxford University Grenadines E?q)edition, wiiich set out to describe the butterflies of the tiny Grenadine islands in the West Indies. West Indian butterflies have a proud, if little recognised, place in the history of island biogeography. Eugene Munroe was patron to the OU Grenadines Expedition and it was in his doctoral thesis (Munroe, 1948) that the modem theory of island biogeography was first formulated (Gilbert, 1984; Brown and Lomolino, 1989; Wilkinson, 1993). In 1948 West Indies butterflies were inconq)letely known and since then many new species have been described and new island records added. Norman Riley was the first to bring together the whole West Indian butterfly fauna (Riley, 1975). This has recently been updated in an even more comprehensive account of the region’s butterflies (Smith et al., 1994). These studies, and the many investigations of individual islands and butterflies on which they are based, form a solid foundation for the work presented here. With the application of genetic techniques, this thesis begins a new era in the study of West Indian butterflies. Such genetic studies might finally resolve some of the questions which have long vexed West Indian lepidopterists. Maybe West Indian butterflies, which 10 were at the forefront of classical island biogeography, will also be in the vanguard of genetical island biogeography. This thesis is rooted in classical island biogeography and opens with an updated examination of the species richness of West Indian butterflies. Based on the data from his book (Smith et ai, 1994) David Spencer Smith and I put together hsts of species numbers and physical variables for many of the West Indies. I present and analyse this data in Chapter 2. Essentially, this reworks Munroe’s seminal study (Munroe, 1948) and provides an insight into how our perception of the species- area relationship has changed with more data. I examine the influence of various factors on species richness, and ask vdiether island biogeography can be treated as a stochastic process. The results suggest that, in general, the number of butterfly species found on West Indian islands is strongly correlated with their area. This is consistent with the stochastic hypothesis that smaller populations face an increased probabihty o f ‘random’ extinction. However, the species-area relationship could also result from selective (deterministic) extinction or immigration affecting individual species in a variety of different ways. Without an examination of actual species distributions (presence- absence data is not yet available), it is not possible to exclude this alternative. Chapter 2 provides the framework for the following three chapters which deal with island biogeography at a genetic level. 11 In Chapter 3 four butterfly species are examined using allozyme electrophoresis. The survey is set in the context of the vicariance versus dispersal debate v ^ c h has long defined West Indian biogeography (Liebherr, 1988; Woods, 1989). Genetic data provides a new, and potentially powerful tool with which to resolve this controversy. For this study I was assisted in the laboratory by Igor Emelianov and Peter King. The results show that population genetic structure varies greatly among species and that dispersal has been the most important factor in their historical biogeography.
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