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ECOLOGICAL FACTORS EXPLAINING GENETIC DIFFERENTIATION in APHIDOMORPHA ASSOCIATED with PECAN and WATER HICKORY TREES a Dissertati

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ECOLOGICAL FACTORS EXPLAINING GENETIC DIFFERENTIATION in APHIDOMORPHA ASSOCIATED with PECAN and WATER HICKORY TREES a Dissertati ECOLOGICAL FACTORS EXPLAINING GENETIC DIFFERENTIATION IN APHIDOMORPHA ASSOCIATED WITH PECAN AND WATER HICKORY TREES A Dissertation by KYLE EDWARD HARRISON Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Raul F. Medina Committee Members, Thomas J. DeWitt Cecilia Tamborindeguy Aaron M. Tarone Head of Department, David W. Ragsdale May 2017 Major Subject: Entomology Copyright 2017 Kyle Harrison ABSTRACT Host-associated differentiation (HAD) is a form of ecologically mediated host-race formation between parasite populations. Since HAD can ultimately lead to speciation, it has been proposed as a way to account for the vast species diversity observed in parasitic arthropods. However, the importance of HAD to species diversity is unclear because the factors explaining the occurrence of HAD are only partially understood. Still, there are several examples of parasite-host case study systems for which there is a known cause of reproductive isolation between host-associated parasite populations. Thus, several biological and ecological factors (e.g., immigrant inviability or allochrony) have been proposed as explanatory factors for HAD occurrence. The body of research presented here represents the first quantitative assessment of the generalized relationship between HAD occurrence and the incidence of the proposed explanatory factors. This research was supported by field experiments that assessed the co-occurrence of HAD and particularly important explanatory factors. These experiments were conducted in a community of Aphidomorpha species living on pecan and water hickory trees. I found that HAD can be explained in general based on the incidence of specific explanatory factors (i.e. immigrant inviability, gall-making, short generation times, volatile preference, morphological differentiation, and host-shifting opportunities). These factors were used to create a hierarchy of conditional probabilities that can successfully separate the presence of HAD from its absence. The field experiments corroborated that the occurrence of HAD is correlated with immigrant inviability as well as allochrony. ii DEDICATION This dissertation is dedicated to the people who loved and supported me throughout my doctorate. Thank you, Tammy Buffington, for being a devoted mother and mentor. Thank you, Steve Buffington, for always being there for me. Thank you, Lindsay Orlando, for sheltering me from hunger. Thank you, Chris Owens, for being my best friend for life. And thank you, Jordan Goebel, for your emotional support and your unwavering belief in me. iii ACKNOWLEDGEMENTS This dissertation would not have been possible without Dr. Raul F. Medina’s mentorship and limitless patience. I also thank Drs. Cecilia Tamborindeguy, Thomas J. DeWitt, and Aaron M. Tarone for allowing me to lean on their expertise throughout my doctorate program. I also extend special thanks to all of my lab mates, past and present. In particular, thanks go to Dr. Aaron Dickey for paving the way for this research by producing preliminary results within the pecan and water hickory Aphidomorpha community. Also, thank you, Drs. Josephine Antwi and Suhas Vyavhare, for your friendships and incredibly helpful advice. For helping me practice for both my preliminary examinations and defense talk, I want to thank Dr. Jason Carbaugh, Jocelyn Holt, Mackenzie Tietjen, and Crystal Wright. Lastly, thanks go to the Texas EcoLab program for providing invaluable funding opportunities. iv CONTRIBUTORS AND FUNDING SOURCES Contributors This work was reviewed by a dissertation committee consisting of Associate Professor Raul F. Medina (Committee Chair) and Associate Professors Cecilia Tamborindeguy and Aaron M. Tarone of the Department of Entomology and Associate Professor Thomas J. DeWitt of Wildlife & Fisheries. All work for the dissertation was completed by Kyle Harrison, under the advisement of Raul F. Medina. The genetic characterizations of pecan and water hickory Aphidomorpha supplied in Chapter I were analyzed in a collaboration between Kyle Harrison, Raul F. Medina of the Department of Entomology and Aaron M. Dickey and Larry J. Grauke of the USDA ARS and were published in Entomologia Experimentalis et Applicata, 2017. Funding Sources This work was made possible in part by the Texas Ecolab Program. Partial financial support for this research was also provided by USDA Hatch funding (TEX09185, RFM). The contents of this dissertation are solely the responsibility of the authors and do not necessarily represent the official views of the Braun & Gresham, PLLC or the USDA. v NOMENCLATURE B/CS Bryan/College Station HAD Host-associated differentiation TAMU Texas A&M University USDA ARS United States Department of Agriculture: Agricultural Research Service PCA Principal Component Analysis CCA Canonical Correspondence Analysis MANOVA Multiple Analysis of Variance vi TABLE OF CONTENTS Page ABSTRACT .............................................................................................................. ii DEDICATION .......................................................................................................... iii ACKNOWLEDGEMENTS ...................................................................................... iv CONTRIBUTORS AND FUNDING SOURCES ..................................................... v NOMENCLATURE .................................................................................................. vi TABLE OF CONTENTS .......................................................................................... vii LIST OF FIGURES ................................................................................................... ix LIST OF TABLES .................................................................................................... x CHAPTER I INTRODUCTION TO RESEARCH AND STUDY SYSTEM ..... 1 Study System Description ................................................................................... 6 CHAPTER II EXPLAINING THE OCCURRENCE OF HOST-ASSOCIATED DIFFERENTIATION: A QUANTITATIVE LITERATURE REVIEW .................. 15 Synopsis ........................................................................................................ 15 Introduction ........................................................................................................ 16 Methods ........................................................................................................ 25 Results ........................................................................................................ 32 Discussion ........................................................................................................ 37 CHAPTER III ASSESSING THE ROLE OF IMMIGRANT INVIABILITY IN A CASE OF PARTIAL HOST-ASSOCIATED DIFFERENTIATION (HAD) INVOLVING THE BLACK-MARGINED APHID, MONELLIA CARYELLA ....... 46 Synopsis ........................................................................................................ 46 Introduction ........................................................................................................ 47 Methods ........................................................................................................ 52 Results ........................................................................................................ 57 Discussion ........................................................................................................ 63 vii CHAPTER IV ALLOCHRONY AND HOST-ASSOCIATED DIFFERENTIATION IN APHIDS ........................................................................... 71 Synopsis ........................................................................................................ 71 Introduction ........................................................................................................ 72 Methods ........................................................................................................ 77 Results ........................................................................................................ 79 Discussion ........................................................................................................ 81 CHAPTER V CONCLUSIONS AND FUTURE DIRECTIONS ......................... 90 REFERENCES ........................................................................................................ 96 APPENDIX ........................................................................................................ 133 viii LIST OF FIGURES FIGURE Page 1 Population Genetic Structuring of Pecan and Water Hickory Aphidomorpha Based on AFLP’s, Reprinted with Permission from Medina, Dickey, Harrison, and Miller (2017) ............................................... 7 2 CCA of HAD Occurrence Based on the Incidence of Biological and Ecological Factors ......................................................................................... 34 3 Hierarchy of Conditional Probabilities Separating HAD Presence from Absence Based on the Incidence of Biological and Ecological Factors ....... 36 4 Adult Longevity and Fecundity during Reciprocal Transplant Experiments Involving Host-Associated Black-Margined Aphids ............... 61 5 CCA of SNPs Characterizing Generalist and Specialist Black-Margined Aphid Populations ......................................................................................... 62 6 Population Density of Three Pecan and Water Hickory Aphididae
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