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Ecological Divergence and Speciation in Heliconius Cydno and H Ecological divergence and speciation in Heliconius cydno and H. melpomene by Russell Edward Naisbit A thesis submitted for the degree of Doctor of Philosophy of the University of London September 2001 Department of Biology University College London To my family, for their support and encouragement throughout this crazy endeavour 2 “It is hardly an exaggeration to say, that whilst reading and reflecting on the various facts given in this Memoir, we feel to be as near witnesses, as we can ever hope to be, of the creation of a new species on this earth.” Charles Darwin, Natural History Review: Quarterly Journal of Biological Science, 1863. From a review of “Contributions to an Insect Fauna of the Amazon Valley,” in which Henry Walter Bates gave an adaptive explanation for mimicry in Amazonian butterflies and argued that variation in mimicry might cause speciation 3 Abstract We are in the midst of a renaissance in speciation research. There is a return to Darwin’s belief in the role of natural selection in driving speciation, after a lengthy focus on geographic isolation and hybrid sterility. Here I describe the ecological, behavioural, and genetic bases of speciation in Heliconius cydno and Heliconius melpomene (Lepidoptera: Nymphalidae). The two species are sympatric in tropical rainforest across most of Central America and the foothills of the Andes. Ecological differentiation allows coexistence of these sister species despite rare hybridisation. Divergence in microhabitat and larval host plant use has reduced both the potential for gene flow and for competition. In Panama H. cydno uses most Passiflora species in closed canopy forest, whilst H. melpomene is restricted to disturbed habitats, and to Passiflora menispermifolia. This ecological differentiation probably generated selection for the key step in their speciation: divergence in warning colour pattern. Both species are unpalatable but are members of different Müllerian mimicry rings that segregate between the two habitats. In Panama H. cydno is black and white and mimics H. sapho, while H. melpomene is black, red and yellow and mimics H. erato. This shift in mimicry reduced both the survival and production of hybrids, due to selection against their non-mimetic pattern, and coevolution of mate choice with colour pattern. Major genes are involved in the control of colour pattern differences, including several homologous with inter-racial variation within each species. Two other postmating barriers affect the reproductive success of hybrids. Disruptive sexual selection acts against them, as both sexes of F1 have poor mating success with the parental species. Following Haldane’s rule, female F1 hybrids are completely sterile, but males are fully fertile and backcross offspring include fertile females. In this and several recent examples, ecological adaptation has been sufficient to catalyse speciation. 4 Acknowledgements None of these words or caterpillars would have made it through the larval stage without the help of many people in Colombia, Panama and the UK. I am forever indebted to Jim Mallet, my supervisor, for having faith initially, being concerned in the middle, encouragement at the end, and for guidance throughout; to Jim and Chris Jiggins, for their endless re-reads of re-writes, and for nurturing this fledgling tropical biologist while he was floundering about in the undergrowth and getting lost in swamps; to Mauricio Linares for welcoming me into his family during my first weeks in Colombia, for help throughout our stay, and together with Camilo Salazar for data from Colombian H. melpomene; to Maria Teresa Almanza, Luis Beltrán, Margarita Beltrán, Catalina Estrada, Gonzalo Fajardo, Adriana Rojas, Clara Saldamando, and Roxana Yockteng, for making us feel instantly at home in Colombia; to Enrique Bustos, Emigdio Güiza, Marina Ordoñez, Cielo Rocío de Oro, and Norma Pineda, for their help in the Instituto de Genética in Bogota; to Mathieu Joron for history’s most tragicomic short field visit, it was the best of times, it was the worst of times (a cliché that never was so true); to Marcela Porras for making Colombia such a difficult place to leave; to Bernard Hermier for revealing the exact spot at which to catch H. melpomene melpomene in French Guiana, after we’d spent more than a week feeding the mosquitoes; to Richard Woods, Camilla Paresce, Luis Alberto Taylor R., Catalina Estrada, Margarita Beltrán, Lianne O’Donovan, Rebecca Coe, Vanessa Bull, Cris Thompson, and Yaneth Sánchez for saving caterpillars from starvation and humans from boredom on many occasions in Panama; 5 to Catalina Estrada for help in hunting eggs, and for identifying the parasitoids that all too often came out of them; to Vanessa Bull and Cris Thompson for being good friends during my final onslaught down on the farm, and for enduring my brief foray into tropical forestry; to Ziheng Yang for the use of his betabinomial program to analyse sterility data; to the past and present inhabitants of room 407, Alan Bolton, Sam Cotton, Angela Gouge, Claire Grant, and Imogen Hurley, for their friendship and for putting up with my absent-minded wandering; to the Autoridad Nacional del Ambiente (ANAM) for permission to work in Panama; to the Smithsonian Tropical Research Institute for making fieldwork in Panama so simple and rewarding, and especially to Dr Eldredge Bermingham for help during our early days there; to the Biotechnology and Biological Sciences Research Council for my studentship, and the Natural Environment Research Council for the grant to Jim Mallet; and most of all to my family, for their encouragement and support, and for bearing the worry of this adventure during its exotic and desk-bound phases. It is to them that I dedicate this thesis. 6 Declaration The chapters include data from collaborative work, in which I performed all or the major part of the experimental work. All the chapters were written by me, and some may form the basis of co-authored publications of which I will be the first author. Chapter 4 has already been published as: Naisbit, R. E., Jiggins, C. D. & Mallet, J. 2001 Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene. Proc. R. Soc. Lond. B 268, 1849-1854. The appendices contain two papers senior authored by Dr Chris Jiggins, but to which I contributed. Appendix 1 describes the effect of divergence in mimetic colour pattern on mate choice in Heliconius cydno and H. melpomene: Jiggins, C. D., Naisbit, R. E., Coe, R. L. & Mallet, J. 2001 Reproductive isolation caused by colour pattern mimicry. Nature 411, 302-305. Appendix 2 describes a novel example of sterility and its genetic basis, in crosses between geographic races of H. melpomene from French Guiana and Panama or Colombia: Jiggins, C. D., Linares, M., Naisbit, R. E., Salazar, C., Yang, Z. H. & Mallet, J. 2001 Sex-linked hybrid sterility in a butterfly. Evolution 55, 1631-1638. Russell Naisbit Prof. James Mallet Candidate Supervisor 7 Contents Abstract .........................................................................................................................4 Acknowledgements.......................................................................................................5 Declaration....................................................................................................................7 Contents ........................................................................................................................8 List of tables................................................................................................................10 List of figures ..............................................................................................................11 Chapter 1 Introduction Ecological divergence and speciation .........................................................................12 Isolation by premating barriers alone ....................................................................13 Postmating barriers ................................................................................................14 Natural selection and speciation.............................................................................16 Reinforcement of premating isolation.....................................................................17 Sexual selection and speciation ..............................................................................18 Species coexistence despite hybridisation...............................................................20 The semipermeable species boundary.....................................................................20 Reversible speciation ..............................................................................................21 Intermediate stages and the possibility of sympatric speciation.............................21 The rate of speciation..............................................................................................22 Heliconius as a model system for speciation ..............................................................22 Heliconius cydno and H. melpomene..........................................................................24 Layout of the thesis .................................................................................................25 References...................................................................................................................26 Chapter 2 Habitat and host use as catalysts for speciation in Heliconius
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