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On the Nature of Genetic Variation in Yellow Monkeyflower (Mimulus Guttatus): Combining Theoretical and Empirical Approaches by Keely Elizabeth Brown

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On the Nature of Genetic Variation in Yellow Monkeyflower (Mimulus Guttatus): Combining Theoretical and Empirical Approaches by Keely Elizabeth Brown On the nature of genetic variation in yellow monkeyflower (Mimulus guttatus): combining theoretical and empirical approaches By Keely Elizabeth Brown Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. Chair: John K. Kelly T. Christopher Gamblin Lena Hileman Maria E. Orive Benjamin Sikes Date Defended: 28 June 2019 ii The dissertation committee for Keely Elizabeth Brown certifies that this is the approved version of the following dissertation: On the nature of genetic variation in yellow monkeyflower (Mimulus guttatus): combining theoretical and empirical approaches Chair: John K. Kelly Date Approved: 15 July 2019 iii Abstract Evolution via natural selection requires standing variation in a population while simultaneously diminishing it at loci under selection, a paradox that continues to vex evolutionary biologists. The work presented here contributes to our understanding of how variation can be maintained by selection, why decreasing genetic variation is detrimental on an individual level, and how genetic variation can have complicated effects on fitness-related phenotypes. Chapter one demonstrates that antagonistic pleiotropy caused by a fitness tradeoff between polygenic traits can maintain variation at a single locus by generating emergent overdominance. The results are surprisingly robust to perturbations in the underlying assumptions about random mating and environmental heterogeneity. Chapter two provides an explanation for how mating system can influence the maintenance of variation. Inbreeding depression in the Iron Mountain population of yellow monkeyflower (Mimulus guttatus) is potentially severe enough to maintain outcrossing and is also predicted by the load of rare alleles carried by a genotype. Chapter three illustrates the complex relationships between genotype and phenotype that are likely underappreciated in typical QTL mapping or GWAS approaches, due to tightly linked antagonistic effectors. It provides a mechanism for studying the influence of genetic variation on complex fitness-related phenotypes, like flower size. iv Acknowledgements I want to thank my advisor, JKK, for the support in research and development as a scientist. Thanks to my committee for helping me to develop skills for an academic career. I also want to thank many people, including EEB faculty, grad students, and academic advisors. Though they are too numerous to name in full: Boryana Koseva, Carrie Wessinger, Amanda Katzer, Polina Sterkhova, Katie Sadler, Lena Hileman, Aniket Sengupta, EEB genetics, current and former members of the Kelly and Hileman labs, the KU Dance department, the KU GSC, Lawrence Parks and Rec, and the CSHL Plant Course. I’ve had an amazing time interacting with everyone, and I’ll miss Lawrence and KU a great deal. Thanks to Rachel Wyman for sitting next to me in Chemistry that one time. I’d like to thank my family, especially my sister, Carlee Nave. Our girls’ trips helped me relax a little during the hardest parts of grad school. Thanks to Nikola, Diva, and Shelldon for the love and support. Finally, I’d like to dedicate this dissertation to my parents, Scott Brown and Cheryl Gray, without whom none of this would have been possible. I love you both! v Table of Contents Abstract .................................................................................................................................... iii Acknowledgements ................................................................................................................... iv List of Figures .......................................................................................................................... vii List of Tables .......................................................................................................................... viii Introduction ................................................................................................................................1 Chapter 1: Antagonistic pleiotropy can maintain fitness variation in annual plants ......................4 Abstract...................................................................................................................................5 Introduction.............................................................................................................................6 Theory ....................................................................................................................................9 Discussion ............................................................................................................................. 22 Conclusion ............................................................................................................................ 29 Supplemental Appendix ........................................................................................................ 31 Supplemental Figures and Tables .......................................................................................... 34 Chapter 2: Severe inbreeding depression is predicted by the “rare allele load” in Mimulus guttatus ..................................................................................................................................... 45 Abstract................................................................................................................................. 46 Introduction........................................................................................................................... 47 Methods ................................................................................................................................ 49 Results .................................................................................................................................. 54 Discussion ............................................................................................................................. 60 Supplemental Appendix 1 ..................................................................................................... 65 Supplemental Figures ............................................................................................................ 66 vi Supplemental Tables ............................................................................................................. 71 Chapter 3: Dissection of a flower size QTL in Mimulus guttatus reveals a complex path from genotype to phenotype .............................................................................................................. 76 Introduction........................................................................................................................... 77 Methods ................................................................................................................................ 80 Results .................................................................................................................................. 86 Discussion ........................................................................................................................... 100 Supplementals ..................................................................................................................... 104 References .............................................................................................................................. 114 vii List of Figures 1.1- Conditions for polymorphism with antagonistic pleiotropy…………………………………12 1.2- Function plots depicting emergent overdominance………………………………………….15 1.3- Assortative mating…………………………………………………………………………..21 1.4- Spatial environmental variability……………………………………………………………27 2.1- Effect of rare allele load and heterozygosity on fitness……………………………………..55 2.2- Effect of rare allele load on greenhouse growth…………………………………………….57 2.3- Nonuniform distribution of rare alleles across the genome…………………………………59 3.1- Linkage disequilibrium of polymorphisms in QTL8………………………………………...88 3.2- Complex and varied effects within QTL8…………………………………………………....94 3.3- Allele-specific expression depicting cis- or trans- regulation……………………………….96 3.4- Effect of knocking out QTL8 orthologs in Arabidopsis thaliana……………………………99 viii List of Tables 3.1- Effect of QTL8 gene expression on life-history traits……………………………………....90 3.2- Effect of genotype on life-history traits……………………………………………………..91 3.3- Effect of genotype on QTL8 gene expression………………………………………………92 3.4- ANCOVA analysis of effect of either genotype or expression on life-history traits……….93 3.5- T-tests for allele-specific expression……………………………………………………..…97 1 Introduction One fundamental paradox in the theory of evolution is that natural selection requires standing variation in a population but diminishes that variation at loci under selection. New mutation and migration are not sufficient to guarantee enough standing variation for a population to either adapt to a changing environment or colonize a new one (Lewontin 1974). Prior to the development of DNA sequencing, and its subsequent widespread use in diagnosing genetic variants in populations, three theories arose to predict the presence and extent of variation and allelic diversity we should expect. Those subscribing to the Classical school of population genetics expected genetic polymorphism to be a rare occurrence, and a transient property of a locus under selection (Muller 1950). In
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