DIVERSIFICATION ON ISLANDS: BULIMULID LAND SNAILS OF GALÁPAGOS by Christine E. Parent M.Sc., Carleton University 2000 B.Sc., McGill University 1998 THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY In the Department of Biological Sciences © Christine E. Parent 2008 SIMON FRASER UNIVERSITY Summer 2008 All rights reserved. This work may not be reproduced in whole or in part, by photocopy or other means, without permission of the author. APPROVAL Name: Christine Parent Degree: Ph.D. Title of Thesis: Diversification on islands: bulimulid land snails of Galápagos Examining Committee: Chair: Dr. L. Bendell-Young, Professor ________________________________________ Dr. B. Crespi, Professor, Senior Supervisor Department of Biological Sciences, S.F.U. ________________________________________ Dr. A. Mooers, Associate Professor Department of Biological Sciences, S.F.U. ________________________________________ Dr. M. Hart, Associate Professor Department of Biological Sciences, S.F.U. ________________________________________ Dr. F. Breden, Professor Department of Biological Sciences, S.F.U. ________________________________________ Dr. I. Côté, Professor Department of Biological Sciences, S.F.U. Public Examiner ________________________________________ Dr. R. Gillespie, Professor Department of Environmental Science, Policy, and Management, University of California, Berkeley Date Defended/Approved: July 28, 2008_____________________________ ii ABSTRACT Adaptive radiation is one of the main processes involved in the formation of the world’s organic diversity. Thus, understanding the processes involved in adaptive radiation becomes a key component of the study of evolutionary biology. The study of adaptive radiation entails a wide range of questions involving various aspects of phylogeny, biogeography, adaptation, and speciation. One of many approaches to a problem as broad as this is to seek an understanding of a small and simplified part of it. Islands provide this simplicity, naturally. The aim of the present work is to reach a better understanding of diversification in adaptive radiations, using Galápagos endemic bulimulid land snails as model system. First, I combined phylogenetics and biogeographical analyses to partition island species diversity by its originating processes: between-island colonization and within-island speciation. The results show that diversification of Galápagos bulimulid land snails has been driven by a combination of geographic factors (island age, size, and location), which affect colonization patterns, and ecological factors, such as plant species diversity, that foster within-island speciation. I then tested the classic evolutionary theory of ecological opportunity, which proposes that the combination of increase in wealth of resources and decrease of potential enemies promotes diversification in lineage colonizing previously empty adaptive zones. I show that ecological opportunity predicts the extent of intraspecific phenotypic variation, explicitly linking the role of competition from congeners and iii the heterogeneity of resources to the extent of intraspecific phenotypic divergence as adaptive radiation proceeds. Finally, I tested for a fit between the phenotypes of diversifying species and their environments. I tested for such a phenotype-environment association (1) across the adaptive radiation of Galápagos bulimulid land snail species, and (2) within one species, Bulimulus reibischi. I found that shell morphology has evolved across species repeatedly on different islands in response to moisture gradient in the same direction as within- species morphological variation among populations of B. reibischi. The parallel association between environment and phenotype both above and below the species level suggests that ecologically-based selection is involved in diversification at both population and species levels in this adaptive radiation. Keywords: adaptive radiation, diversification, ecological opportunity, Galápagos Islands, island biogeography, phenotypic variation, species richness. iv ACKNOWLEDGEMENTS This work would not have been possible without the support and encouragement of a long list of people. Dr. Bernard Crespi, my supervisor, for his endless patience and constant sound advice. The other members of my committee: Arne, there from the start, and Mike and Felix, welcomed additions later on. Together with Bernie, they provided an incredible source of support and inspiration. All members of the FAB*-lab at SFU, simply the best research group a graduate student in evolutionary biology could wish to be part of. In particular, former and current members of the Crespi Lab, for providing a stimulating and fun environment in which to learn and to live. My time at SFU would not have been as enjoyable without you. The staff of the Charles Darwin Research Station and Parque Nacional de Galápagos for their continued support and collaboration. Particularly Charlotte Causton and Lazaro Roque, as well as the team of Terrestrial Invertebrates at the Charles Darwin Research Station. My collaborators for chapter 1, Ken Petren and Gisella Caccone. The numerous people that helped gathering field or lab data: Sampson Wu, Clair Keays, Deborah Austin, Eugénie Parent, Louis de Redon, MarieLou Poisson, v Carole Bender, Novalino Castillo, Pedro Castillo, and Tom Poulsom. Shannon Wood and Heather Robertson from the Archaeology Department for help with the shell radiographs. I would also like to thank Guy, for the very special person he is, and for the incredible amount of understanding he had with me over the past few years. And last but not least, my parents, for creating an environment in which following this path seemed so natural. I would like to dedicate this work to my dad, who taught me that asking the question can often be more important than finding an answer. vi TABLE OF CONTENTS Approval ..............................................................................................................ii Abstract ..............................................................................................................iii Acknowledgements ............................................................................................v Table of Contents..............................................................................................vii List of Figures .....................................................................................................x List of Tables......................................................................................................xi Chapter 1: COLONIZATION AND DIVERSIFICATION OF GALÁPAGOS TERRESTRIAL FAUNA: A PHYLOGENETIC AND BIOGEOGRAPHICAL SYNTHESIS..........................................................................................................1 ABSTRACT........................................................................................................1 INTRODUCTION ...............................................................................................2 THE GALÁPAGOS ARCHIPELAGO..................................................................3 Geographic setting .........................................................................................3 Geological history...........................................................................................6 Biogeography and ecology.............................................................................7 Endemism and diversification.........................................................................8 ORIGINS OF ENDEMICS AND AGE OF GALÁPAGOS FAUNA.....................11 Source of the fauna ......................................................................................11 Age of the fauna ...........................................................................................16 TIMING AND SEQUENCE OF COLONIZATION AND SPECIATION..............18 Speciation between islands..........................................................................23 Speciation within islands ..............................................................................27 Dynamics of species diversification..............................................................32 FUTURE PROSPECTS FOR EVOLUTIONARY RESEARCH ON GALÁPAGOS ISLANDS ...................................................................33 CONSERVATION AND THE ROLE OF EVOLUTIONARY GENETICS IN GALÁPAGOS RESEARCH ..........................................................34 Chapter 2: SEQUENTIAL COLONIZATION AND DIVERSIFICATION OF GALÁPAGOS’ ENDEMIC LAND SNAIL GENUS BULIMULUS (GASTROPODA, STYLOMMATOPHORA)........................................................37 ABSTRACT......................................................................................................37 INTRODUCTION .............................................................................................38 MATERIALS AND METHODS .........................................................................47 Field sampling ..............................................................................................47 DNA preparation, amplification, and sequencing..........................................48 vii Phylogenetic analyses..................................................................................49 Test of island assemblage monophyly..........................................................51 Colonization sequence analysis ...................................................................53 Biogeographical