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Causes and Consequences of Recombination Rate Variation By Causes and Consequences of Recombination Rate Variation by Caitlin Suzanne Smukowski Heil Department of Biology Duke University Date:_______________________ Approved: ___________________________ Mohamed Noor, Supervisor ___________________________ John Willis ___________________________ Storrs Mitchell-Olds ___________________________ Thomas Petes ___________________________ Corbin Jones Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2014 ABSTRACT Causes and Consequences of Recombination Rate Variation by Caitlin Suzanne Smukowski Heil Department of Biology Duke University Date:_______________________ Approved: ___________________________ Mohamed Noor, Supervisor ___________________________ John Willis ___________________________ Storrs Mitchell-Olds ___________________________ Thomas Petes ___________________________ Corbin Jones An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2014 Copyright by Caitlin Suzanne Smukowski Heil 2014 Abstract Recombination is the process in which genetic material is exchanged between one's homologous chromosome pairs during egg or sperm development (meiosis). Recombination is necessary for proper segregation of chromosomes during meiosis, and also plays a role in purging deleterious mutations, accelerating adaptation, and influencing the distribution of genomic features over evolutionary time. While recombination is clearly an important process, recombination rate is known to vary within and between individuals, populations, and species. Furthermore, what causes this variation remains relatively unknown. Using empirical and sequenced based estimates of recombination rate for the closely related species Drosophila pseudoobscura and Drosophila miranda , I seek to understand where recombination happens across the genome, to what extent recombination changes between species, and what genomic features are responsible for these changes. These data will deepen our understanding of mechanisms determining the recombination landscape, and shed light on generalized patterns and exceptions of recombination rate variation across the tree of life. iv Contents Abstract ......................................................................................................................................... iv List of Tables .............................................................................................................................. viii List of Figures ............................................................................................................................... ix Acknowledgements ...................................................................................................................... x 1. Recombination rate variation in closely related species ...................................................... 1 Introduction ............................................................................................................................. 1 Determinants and Correlates ................................................................................................ 4 Molecular Evolutionary Consequences of Recombination Rate Variation .................... 8 Conservation and Divergence of Recombination .............................................................. 9 How does the methodology by which recombination is measured affect estimates of recombination rate? ............................................................................................................ 10 Why would we see conservation of recombination rates between some species and not others? ........................................................................................................................... 13 Why would we see recombination rate conservation at some scales and not others? ............................................................................................................................................... 15 Should we expect to see conservation between closely related species?.................... 18 Conclusions ........................................................................................................................... 20 2. Recombination modulates how selection affects linked sites in Drosophila .................... 33 Smukowski Heil Contribution ............................................................................................ 33 Introduction ........................................................................................................................... 33 Materials and Methods ........................................................................................................ 40 Results .................................................................................................................................... 49 v General Summary of Recombination Data: Fine-Scale Maps ...................................... 49 General Summary of Recombination Data: Ultrafine-Scale Maps .............................. 53 Recombination Rate Comparison between Maps .......................................................... 54 Diversity, Divergence, and Recombination .................................................................... 59 Recombination and Selection ............................................................................................ 63 Discussion .............................................................................................................................. 69 3. Zinc finger binding motifs do not explain recombination variation within or between species of Drosophila .................................................................................................................. 78 Introduction ........................................................................................................................... 78 Materials and Methods ........................................................................................................ 83 Results .................................................................................................................................... 89 Prdm9 homology ................................................................................................................ 89 Candidate protein analysis ............................................................................................... 91 A comprehensive search for a zinc finger binding sequence motif ............................ 96 Differences in motif occurrences do not account for changes in recombination landscapes between closely related species .................................................................... 97 Sequence motifs .................................................................................................................. 99 A validation of our approach using human recombination data .............................. 100 Discussion ............................................................................................................................ 100 4. No detectable effect of DNA methyltransferase DNMT2 on meiotic recombination . 106 Introduction ......................................................................................................................... 106 Materials & Methods .......................................................................................................... 110 Results .................................................................................................................................. 115 vi Recombination across a euchromatic region ................................................................ 115 Discussion ............................................................................................................................ 116 5. The fine scale recombination landscape in two species of Drosophila ......................... 120 Introduction ......................................................................................................................... 120 Materials and Methods ...................................................................................................... 124 Results and Discussion ...................................................................................................... 128 LD-based recombination maps are good estimates of empirical recombination maps ............................................................................................................................................. 128 Between species recombination rate comparison ........................................................ 130 Distribution of recombination rate across the genome ............................................... 133 Conclusions ......................................................................................................................... 137 Works Cited ............................................................................................................................... 138 Biography ................................................................................................................................... 175 vii List of Tables Table 1: Relationships between recombination rate and measures of diversity and divergence ...................................................................................................................................
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