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Natural Hybridization and Speciation in Toads of the Anaxyrus

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Natural Hybridization and Speciation in Toads of the Anaxyrus NATURAL HYBRIDIZATION AND SPECIATION IN TOADS OF THE ANAXYRUS AMERICANUS GROUP by BRIAN E. FONTENOT Presented to the Faculty of the Graduate School of The University of Texas at Arlington in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY THE UNIVERSITY OF TEXAS AT ARLINGTON August 2009 Copyright © by Brian E. Fontenot 2009 All Rights Reserved ACKNOWLEDGMENTS Several individuals, organizations, and institutions assisted me during my time at the University of Texas at Arlington (UTA) and this work would not have been possible without them. Financial support for this project was provided by my Ph.D. advisor, Paul Chippindale, my former Ph.D. advisor, Jeremy Marshall, and a Phi Sigma Biological Society Research Grant I received in 2006. Additionally, the Department of Biology at UTA supported me with a Graduate Teaching Assistantship for my entire tenure, allowing me to obtain valuable teaching experience, which I have greatly enjoyed. I would like to thank the following individuals and academic institutions for donating tissue samples and allowing me to examine preserved specimens: Jonathan Campbell, Paul Ustach, and Carl Franklin at the University of Texas at Arlington Amphibian and Reptile Diversity Research Center, David Cannatella and Travis LaDuc at the Texas Natural History Collection, Gregory Watkins-Colwell at the Peabody Museum of Natural History, Kenneth Kozak, Benjamin Lowe, and Tony Gamble at the Bell Museum of Natural History, David Green and Michele Steigerwald at the Canadian Museum of Natural History, and Leslie Rissler at the University of Alabama Herpetological Collection. I would also like to thank my committee members, Paul Chippindale, Jonathan Campbell, Dan Formanowicz, Pawel Michalak, Jeff Demuth, and Esther Betran for all of their guidance and help during my time at UTA. I have been a very independent student, iii probably to a fault, but each of my committee members has helped me when I needed them and I am thankful. I am extremely grateful to my fellow graduate students and friends: Jesse Meik, John Malone, Matt Watson, Michelle Lawing, Walter Schargel, Nate Bendik, Kerri Mitchell, Amie Treuer, Chad Larson, Matt Gifford, Roberto Brenes, Robert Makowsky, Corey Roelke, Christian Cox, John Morse, Charles Tracy, Chris Hamilton, Jeff Streicher, Thomas Eimermacher, Claudia Marquez, Sarah Schaak, Claudio Casola, Ben Anders, Rebecca Calisi, and Amy Carrillo. These individuals have all contributed to this work by providing tissue samples, helping out with laboratory work, consulting on statistical issues, and discussing my sometimes confusing results, but their most important contribution is their friendship. I would also like to thank Jennifer Pramuk, Gregory Pauly, Laura Vogel, David Green, and Norman Johnson for their invaluable advice and assistance with various aspects of this work. The UTA staff, Linda Taylor, Gloria Burlingham, Peggy Fisher, Belinda Zollotuchen, and Morris Anthony, have helped me so many times in so many ways that it is impossible to measure. Without their help, I would not have been able to finish my dissertation and I am eternally grateful. One individual who deserves special recognition is Carol Moulton. Carol helped me out in so many ways when I needed it most. I will always be grateful for our time together and look forward to a long friendship. Finally, I would like to thank my parents, John and Linda Fontenot, whose love and support allowed me to pursue my dreams. July 17, 2009 iv ABSTRACT NATURAL HYBRIDIZATION AND SPECIATION IN TOADS OF THE ANAXYRUS AMERICANUS GROUP Brian E. Fontenot, Ph.D. The University of Texas at Arlington, 2009 Supervising Professor: Paul T. Chippindale The goal of speciation research is to elucidate the processes that lead to the formation of new species. Examining natural hybridization and the evolution of reproductive isolating barriers provides an opportunity to understand the dynamic processes that occur before, during, and after speciation events. Here, I use true toads of the Anaxyrus americanus group to examine the effects of natural hybridization on 1) the evolution of reproductive isolation using previously published laboratory hybridization data on multiple species within the family Bufonidae, 2) morphological variation using morphometric analysis of known Anaxyrus americanus group hybrids, and 3) molecular variation and genetic population structure in the Anaxyrus americanus group using AFLP markers. v First, postzygotic isolation shows a positive correlation with genetic divergence in bufonids, suggesting that diverging species will become increasingly isolated over time, as seen in other organisms. Toads also display some unusual patterns of reproductive isolation in that fertilization rate is not correlated with genetic divergence. Haldane’s rule for inviability, strictly obeyed in most taxa, is followed in only 56% of crosses with females the affected sex in 70% of these cases. These results suggest that the homomorphic sex chromosomes seen in true toads and/or maternal effects may play a role in the unusual results regarding Haldane’s rule for inviability. Examining offspring for adherence to Haldane’s rule for sterility revealed that only males were affected and degree of ploidy in hybrid offspring does not appear to predict sterility. Second, laboratory-produced hybrid offspring between members of the Anaxyrus americanus group can readily be distinguished from putative parental individuals raised under the same laboratory conditions as well as putative parentals collected from current natural populations. Using discriminant function analysis of morphometric characters, hybrid individuals were correctly classified in 84.3% of cases and putative parental individuals were correctly classified in 99.4% of cases. Hybrids deviated from parental species in aspects of cranium and forelimb morphology. Interestingly, hybrids did not possess morphological traits intermediate between that of their respective parental species; instead they display substantial morphological changes distinguishing them from either parental species. Transgressive segregation in morphological traits due to dominance effects at loci involved in complementary gene action could potentially vi explain these results, although further research is needed before any firm conclusions can be made. Finally, genetic analysis of 100 Amplified Fragment Length Polymorphism (AFLP) loci revealed discrete population structure within and among species, but species in close proximity sharing similar male advertisement calls displayed high levels of gene flow between populations. These results suggest that species in the Anaxyrus americanus group may exist as both distinct populations and as subdivided metapopulations connected by recent or ongoing gene flow, possibly due to natural hybridization. Isolation by distance and prezygotic isolating mechanisms appear to be the primary determinants of population structure within these species. vii TABLE OF CONTENTS ACKNOWLEDGMENTS..................................................................................................iii ABSTRACT ........................................................................................................................v LIST OF ILLUSTRATIONS .............................................................................................ix LIST OF TABLES ...........................................................................................................xiii CHAPTER PAGE 1. INTRODUCTION..................................................................................................1 2. HYBRIDIZATION AND REPRODUCTIVE ISOLATION IN BUFONIDS.......................................................................................................9 3. MORPHOMETRIC ANALYSIS OF HYBRIDIZATION IN THE ANAXYRUS AMERICANUS GROUP .........................................................35 4. AFLP ANALYSIS OF THE ANAXYRUS AMERICANUS GROUP....................52 5. CONCLUSIONS AND IMPLICATIONS ...........................................................88 APPENDIX A. TABLES AND FIGURES...................................................................................96 B. SPECIMENS EXAMINED IN AFLP ANALYSES .........................................168 C. SPECIMENS EXAMINED IN MORPHOLOGICAL ANALYSES ................175 LITERATURE CITED....................................................................................................194 BIOGRAPHICAL INFORMATION ..............................................................................210 viii LIST OF ILLUSTRATIONS Figure Page A.1 Geographic distribution of the Anaxyrus americanus group........................................97 A.2 Hypothesis of interspecific relationships in the Anaxyrus americanus group .............98 A.3 Scatterplot of postzygotic isolation versus genetic distance for both (A) uncorrected and (B) corrected datasets ....................................................102 A.4 Scatterplots of (A) fertilization (B) hatching (C) larvae and (D) metamorphosis versus genetic distance ..........................................................103 A.5 Boxplot of the relationship between genetic divergence and developmental stage reached .................................................................................104 A.6 Boxplot of the relationship between genetic divergence and negatively affected sex in hybrid offspring ...........................................................105 A.7 Plot of the first two discriminant functions
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