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Ecological Speciation with Gene Flow in Neodiprion Pinetum and N. Lecontei

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University of Kentucky UKnowledge Theses and Dissertations--Biology Biology 2020 FROM GENES TO SPECIES: ECOLOGICAL SPECIATION WITH GENE FLOW IN NEODIPRION PINETUM AND N. LECONTEI Emily E. Bendall University of Kentucky, [email protected] Author ORCID Identifier: https://orcid.org/0000-0003-2524-088X Digital Object Identifier: https://doi.org/10.13023/etd.2020.221 Right click to open a feedback form in a new tab to let us know how this document benefits ou.y Recommended Citation Bendall, Emily E., "FROM GENES TO SPECIES: ECOLOGICAL SPECIATION WITH GENE FLOW IN NEODIPRION PINETUM AND N. LECONTEI" (2020). Theses and Dissertations--Biology. 62. https://uknowledge.uky.edu/biology_etds/62 This Doctoral Dissertation is brought to you for free and open access by the Biology at UKnowledge. It has been accepted for inclusion in Theses and Dissertations--Biology by an authorized administrator of UKnowledge. For more information, please contact [email protected]. STUDENT AGREEMENT: I represent that my thesis or dissertation and abstract are my original work. Proper attribution has been given to all outside sources. I understand that I am solely responsible for obtaining any needed copyright permissions. I have obtained needed written permission statement(s) from the owner(s) of each third-party copyrighted matter to be included in my work, allowing electronic distribution (if such use is not permitted by the fair use doctrine) which will be submitted to UKnowledge as Additional File. I hereby grant to The University of Kentucky and its agents the irrevocable, non-exclusive, and royalty-free license to archive and make accessible my work in whole or in part in all forms of media, now or hereafter known. I agree that the document mentioned above may be made available immediately for worldwide access unless an embargo applies. I retain all other ownership rights to the copyright of my work. I also retain the right to use in future works (such as articles or books) all or part of my work. I understand that I am free to register the copyright to my work. REVIEW, APPROVAL AND ACCEPTANCE The document mentioned above has been reviewed and accepted by the student’s advisor, on behalf of the advisory committee, and by the Director of Graduate Studies (DGS), on behalf of the program; we verify that this is the final, approved version of the student’s thesis including all changes required by the advisory committee. The undersigned agree to abide by the statements above. Emily E. Bendall, Student Dr. Catherine R. Linnen, Major Professor Dr. David W. Weisrock, Director of Graduate Studies FROM GENES TO SPECIES: ECOLOGICAL SPECIATION WITH GENE FLOW IN NEODIPRION PINETUM AND N. LECONTEI ________________________________________ DISSERTATION ________________________________________ A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the College of Arts and Sciences at the University of Kentucky By Emily Elizabeth Bendall Lexington, Kentucky Director: Dr. Catherine R. Linnen, Associate Professor of Biology Lexington, Kentucky 2020 Copyright © Emily Elizabeth Bendall 2020 https://orcid.org/0000-0003-2524-088X ABSTRACT OF DISSERTATION FROM GENES TO SPECIES: ECOLOGICAL SPECIATION WITH GENE FLOW IN NEODIPRION PINETUM AND N. LECONTEI My dissertation focuses on how differences accumulate across the genome during ecological speciation with geneflow. To do this I used two species of Neodiprion pine sawflies, which are plant-feeding hymenopterans with high host specificity. I used experimental crosses to measure both intrinsic and extrinsic postzygotic isolation and to understand the contribution of specific traits to reproductive isolation. Despite substantial genetic divergence and haploid males in which all recessive incompatibilities should be expressed, I found surprisingly little evidence of intrinsic postzygotic isolation. Recombination in hybrid males may reconstitute viable genotypes and counteract the effects of haploidy in males. Nevertheless, hybrids have drastically reduced fitness due to intermediate host-use traits causing strong extrinsic postzygotic isolation. Together, these results suggest that divergent selection on host-use traits is the primary driver of speciation in these, and likely other, plant-feeding insects. Next, I performed a QTL mapping study of the traits under divergent selection that contribute to extrinsic postzygotic isolation to understand how genetic architecture can constrain or promote speciation and adaptation. I found that opposing dominance between host-choice and host-use traits composes the genetic basis of the earlier detected extrinsic postzygotic isolation. This opposing dominance is part of a growing body of work showing that trait mismatch and not hybrid intermediacy is typically how extrinsic postzygotic isolation is formed. My fourth chapter focuses on how haplodiploid sex determination shapes how populations accumulate differences across the genome during speciation. Using a combination of demographic analysis of pine sawflies, population genetic simulations, and a meta-analysis, I found that compared to diploids, haplodiploids have predictably higher and more variable differentiation across the genome when they diverge in the presence of gene flow. Overall, Neodiprion sawflies present a great opportunity to better understand the genetics of adaptation and speciation. KEYWORDS: Ecological Speciation, Adaptation, Evolutionary Genetics, Neodiprion, Haplodiploidy, Extrinsic Postzygotic Isolation Emily Elizabeth Bendall 04/20/20 Date FROM GENES TO SPECIES: ECOLOGICAL SPECIATION WITH GENE FLOW IN NEODIPRION PINETUM AND N. LECONTEI By Emily Elizabeth Bendall Catherine R. Linnen Director of Dissertation David W. Weisrock Director of Graduate Studies 04/20/2020 DEDICATION To my father, who always inspired me. I will be eternally grateful for all his love and support. ACKNOWLEDGMENTS I would not have been able to complete this dissertation without the help of so many people. Catherine Linnen has been an amazing mentor and has provided me with so much support, guidance, and insights. I truly couldn’t have done this dissertation without her. To all of the undergrads that assisted in the research; Melanie Hurst, Nicole Payne, Anna Sosso, Julian Horn, Ethan Hunt, Hallee Mason, Parisa Shamaei Zadeh, Ndeye Thiaw, Brianna Washington, Kayla Mattingly, and Ally Appel; and all of those that helped with rearing and taking care of the countless sawflies, I wouldn’t have been able to do this research without you. Robin Bagley, Claire O’Quin, Kim Vertacnik, Danielle Herrig, Ashleigh Glover, John Terbot, and Megan Thomas as the Linnen lab has provided so much support through being there to commiserate when something inevitably goes wrong (something always goes wrong), to celebrate with when things finally start working, and for countless pieces of advice. All of you made the Linnen lab a wonderful place to work. The lab environment got even better once we joined with the Weisrock lab a few years ago to form the Super Lab. Thank you to everyone who has made the Super Lab such as success! The Biology department as a whole has been very supportive and have given me many opportunities. I would especially like to thank Jacquie Burke who made sure that all of the critical behind the scenes work got done and that I never missed a deadline. Jacquie’s door was always open and she was a continual source of positivity. Dave Weisrock and Dave Westneat, as directors of graduate studies were both instrumental in making the program run smoothly. Additionally, Dave Weisrock was on my committee with Chuck Fox and Jeremy Van Cleve. My committee provided me with important guidance and insights during my dissertation. My collaborators, Vitor Sousa, Amanda Moehring, Andres Bendesky, and Natalie Niepoth, were absolutely delightful to work with and added so much to my dissertation. I also want to thank all of my funding sources, the University of Kentucky, the biology department, USDA, and NSF for their monetary support. iii The support of my family has been invaluable. Thank you for all ways being there to listen to me and only occasionally telling me to stop talking about my work. I love you all! iv TABLE OF CONTENTS ACKNOWLEDGMENTS ................................................................................................. iii LIST OF TABLES ............................................................................................................. ix LIST OF FIGURES ............................................................................................................ x CHAPTER 1. INTRODUCTION .................................................................................. 1 1.1 ECOLOGICAL SPECIATION..................................................................................... 2 1.2 GENETICS OF ADAPTATION ................................................................................... 6 1.3 GENOME WIDE PATTERNS OF DIVERGENCE ........................................................... 8 1.4 SAWFLIES AS A STUDY SYSTEM .......................................................................... 11 1.5 DISSERTATION OVERVIEW.................................................................................. 12 1.5.1 Chapter 2. Oviposition traits generate extrinsic postzygotic isolation between two pine sawfly species ............................................................................... 12 1.5.2 Chapter 3. Genetic architecture of oviposition traits ......................
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