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The Evolution of Reproductive Divergence in the Sea

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The Evolution of Reproductive Divergence in the Sea The Evolution of Reproductive Divergence in the Sea by Jennifer M. Sunday B.Sc., University of British Columbia, 2002 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biological Sciences Faculty of Science © Jennifer M. Sunday 2012 SIMON FRASER UNIVERSITY Fall 2012 All rights reserved. However, in accordance with the Copyright Act of Canada, this work may be reproduced, without authorization, under the conditions for “Fair Dealing.” Therefore, limited reproduction of this work for the purposes of private study, research, criticism, review and news reporting is likely to be in accordance with the law, particularly if cited appropriately. Approval Name: Jennifer M. Sunday Degree: Doctor of Philosophy (Science) Title of Thesis: The evolution of reproductive divergence in the sea Examining Committee: Chair: Gordon Rintoul, Associate Professor Michael Hart Senior Supervisor Associate Professor Felix Breden Supervisor Associate Professor Elizabeth Elle Internal Examiner Assistant Professor Department of Biological Sciences Michael Hellberg External Examiner Associate Professor, Department of Biological Sciences Louisiana State University Date Defended: October 3, 2012 ii Partial Copyright Licence iii Abstract Understanding how speciation occurs in the ocean is challenging because the high dispersal potential of marine larvae, and the scarcity of absolute physical barriers to their dispersal, suggest that gene flow should slow or prevent the evolution of divergence among populations. However, spatial heterogeneity in gene flow and localized sexual selection are two potential drivers of divergence among marine populations. Here I investigate how gene flow and sexual selection contribute to reproductive divergence in a coastal seastar with a long larval pelagic phase, Patiria miniata. I first use microsatellite markers to assess genetic population structure across the species range along the west coast of North America, and find a genetic disjunction near the central coast of British Columbia consistent with two hypotheses about the effects of historical climate events and contemporary gene flow. I next use an oceanographic dispersal model to assess the extent to which variation in larval dispersal can account for this structure. I find that oceanographic features predict the genetic structure observed better than dispersal distance between populations alone. Given this genetic structure, I next test the hypothesis that fertilization proteins of this broadcast spawner have diversified among the two (northern and southern) populations, as predicted under a hypothesis of sexual conflict. My findings reveal divergent, positive selection in the sperm protein bindin, which suggest that sexual selection has lead to localized divergence at this fertilization compatibility gene. Finally, I test fertilization compatibility between males and females as a function of population source and male bindin genotype. I find that localized coevolution has occurred in the southern population, and that southern females have a greater affinity than northern females for male bindin genotypes found in the south. Together, these findings provide evidence that patterns in larval dispersal and sexual selection can lead to reproductive divergence in a marine species in spite of its high dispersal potential. Characterizing both genetic structure and adaptive molecular evolution among populations is a powerful approach for understanding incipient speciation in the sea. Keywords: Larval dispersal, population genetic structure, gamete compatibility, bindin, positive selection, sexual conflict, reproductive coevolution, reproductive divergence iv I dedicate this work to my parents. My dad has taught me to be infinitely curious, persistently creative and never to stop learning, and my mom has taught me to aim high in all of my endeavours and to handle challenges with grace and integrity. They are both the most wonderful teachers and fantastic friends. v Acknowledgements There are many people to acknowledge for the completion of this work. I thank first my senior supervisor, Mike Hart, who has been infinitely supportive and has provided tremendous guidance towards every chapter of my thesis from conception to completion. Thanks also to Felix Breden who has provided much guidance and advice in the design of projects, analyses, interpretation, and writing. Thanks to Carson Keever for a huge amount of field and laboratory assistance, and very helpful discussions throughout. Thanks also to Susana Patiño for critical support in bindin genotyping and many chats over data collection and interpretation, and to Iva Popovic for helpful discussions and edits. Thanks to each of my coauthors for their various contributions and assistance with writing. Thanks also to Isabelle Côté for guidance and support in early stages of my thesis work, and to my examining committee for helpful comments on my thesis. I wish to thank all the members of FAB* lab for their fantastic guidance. This lab group is a great place to develop as a scientist, and I am extremely grateful for their dependable ability to help clarify ideas, often poignantly and immediately. Thanks especially to Bernie Crespi, Arne Mooers, and Jeffery Joy (and those aforementioned) in this regard. Thanks to Shane Anderson, John and Vicki Pearse, Edmund Sunday, Scott Walker, Morgan Hocking, Joel Harding, Sophia and Olivia Dulvy, the staff at the Bamfield Marine Sciences Centre, and staff at Moresby Explorers for assistance in collection of sea stars. I thank the Natural Sciences and Engineering Research Council of Canada, the Simon Fraser University Graduate Fellowship program, and the Garfield Weston Foundation/B.C. Packers for financial support. I wish to thank my parents for their tremendous support and encouragement. Finally, I thank my fantastic husband, Mike McDermid, for a million useful discussions, encouragement, comic relief, and above all his patience and undying support. vi Table of Contents Approval ............................................................................................................................. ii Partial Copyright Licence .................................................................................................. iii Abstract ............................................................................................................................. iv Acknowledgements ........................................................................................................... vi Table of Contents ............................................................................................................. vii List of Tables ...................................................................................................................... x List of Figures ................................................................................................................... xi Chapter 1. General Introduction ............................................................................... 1 Thesis chapter overview and author contributions ............................................................ 3 References ........................................................................................................................ 7 Chapter 2. Discordant distribution of populations and genetic variation in a sea star with high dispersal potential .......................................... 11 Abstract ........................................................................................................................... 11 Introduction ..................................................................................................................... 12 Methods .......................................................................................................................... 15 Population Sampling .............................................................................................. 15 Genetic Data Collection ......................................................................................... 15 Microsatellites ................................................................................................ 15 mtDNA ........................................................................................................... 15 Introns ........................................................................................................... 16 Quantitative Analysis ............................................................................................. 17 Polymorphism ................................................................................................ 17 Heuristic measures of population structure ................................................... 17 Population differentiation ............................................................................... 18 Gene flow and effective population size ........................................................ 19 Results ............................................................................................................................ 21 Polymorphism ........................................................................................................ 21 Population Structure .............................................................................................. 22 Population differentiation ....................................................................................... 23 Gene Flow and Effective Population
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