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Duke University Dissertation Template Parental Conflict, Parent of Origin Effects, and the Evolution of Hybrid Seed Failure in Mimulus by Jennifer M. Coughlan Department of Biology Duke University Date:_______________________ Approved: ___________________________ John Willis, PhD, Supervisor ___________________________ Kathleen Donohue, PhD ___________________________ Mark Rausher, PhD ___________________________ Mohamed Noor, PhD ___________________________ Thomas Mitchell-Olds 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 2018 i v ABSTRACT Parental Conflict, Parent of Origin Effects, and the Evolution of Hybrid Seed Failure in Mimulus by Jennifer M. Coughlan Department of Biology Duke University Date:_______________________ Approved: ___________________________ John Willis, PhD, Supervisor ___________________________ Kathleen Donohue, PhD ___________________________ Mark Rausher, PhD ___________________________ Mohamed Noor, PhD ___________________________ Thomas Mitchell-Olds 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 2018 i v Copyright by Jennifer M. Coughlan 2018 Abstract The earth is home to roughly 9 million eukaryotic species. The formation and maintenance of this diversity requires the accumulation of barriers to reproduction. One of the most common post-zygotic barriers in plants is hybrid seed inviability (HSI). Despite its commonality, we know relatively little about the genetic mechanisms and evolutionary forces which are responsible for this barrier, particularly in naturally co- occurring species. Here I tested the role of parental conflict in HSI between co-occurring monkey flowers in the M. guttatus species complex. I assessed the strength and directionality of HSI within and between phenotypically described perennial variants of the M. guttatus species complex. I find substantial HSI between two morphologically described variants, M. guttatus and M. decorus, amounting to ~30-50% reproductive isolation (RI). Genetically distinct clades of M. decorus vary in their ability to cross with M. guttatus in both magnitude and direction of RI. Intriguingly, northern and southern clades of M. decorus are also incompatible with one another, showing strong and symmetric hybrid seed inviability. In all cases, HSI is accompanied by parent of origin effects on F1 seed size, consistent with a role of resource allocation to hybrid inviability. Parent of origin effects on reciprocal F1s were not limited to final size. I characterized the developmental trajectory of seeds between M. guttatus and both the northern and southern clades of M. decorus. Hybrid seeds show similar developmental trajectories iv depending on their end fate (i.e. viable vs inviable), despite differing in the maternal and paternal contributors in these crosses. Inviable seeds were characterized by patterns of paternal excess; chaotic and malformed endosperm. Viable hybrid seeds are characterized by maternal excess; limited, and precocious endosperm development. Relatively normal embryo development early on suggests that hybrid seed inviability stems, in part, from malformed endosperm. Lastly, I use a combination of modeling, next generation sequencing, and marker genotyping approaches to determine the genetic architecture and basis of HSI. I find that the genetic basis of HSI is complex, wherein several maternally and paternally inherited nuclear loci interact to cause HSI. In total, I show the presence of multiple perennial species in the M. guttatus species complex. These species show little phenotypic or obvious ecological differentiation, but are genetically unique and have substantial post-zygotic reproductive isolation, namely through the formation of inviable seeds. Patterns of seed development and final size are indicative of parent of origin effects on resource allocation to endosperm. Despite relatively low genetic differentiation for the group, the genetic basis of HSI is quite complex, involving multiple maternally and paternally interacting alleles. Future work will be needed to determine the identities of these genes, as well as patterns of repeatability across the complex. v Dedication For my Grandmother, Helen Marie Coughlan, who introduced me to the importance of game theory at an early age with her uncanny card skills. vi Contents Abstract ......................................................................................................................................... iv List of Tables .............................................................................................................................. xiii List of Figures .............................................................................................................................xiv Acknowledgements ................................................................................................................. xvii Chapter 1: Introduction ................................................................................................................ 1 1.1 Gene Duplications and Translocations ..................................................................... 3 1.2 Genetic Linkage and Hitchhiking ............................................................................. 5 1.3 Compensatory Mutations and Systems Drift .......................................................... 7 1.4 Divergent Ecological Selection .................................................................................. 9 1.5 Mutation Order Speciation in Response to the Environment ............................. 11 1.6 Auto-Immune system [Co]-Evolution .................................................................... 12 1.7 Parental Conflict ........................................................................................................ 15 1.8 Sex Chromosome formation and speciation .......................................................... 19 1.9 Selfish Genetic Elements ........................................................................................... 21 1.10 Recombination-related processes ........................................................................ 27 1.11 Conclusions ............................................................................................................ 30 Chapter 2: The Mimulus guttatus species complex as a model system for the evolution of hybrid inviability and sterility .................................................................................................. 32 2.1 Hybrid Sterility ............................................................................................................... 33 2.2 Hybrid Inviability (late stage) ....................................................................................... 35 2.3 Hybrid Seed Inviability ................................................................................................. 36 vii 2.4 Research Overview ......................................................................................................... 38 Chapter 3: Patterns of hybrid seed inviability in perennials of the Mimulus guttatus sp. complex ........................................................................................................................................ 42 3.1 Introduction ..................................................................................................................... 42 3.2 Materials and Methods .................................................................................................. 46 3.2.1 Phenotypic and genetic survey of M. decorus ........................................................ 46 3.2.2 Crossing survey between M. guttatus and M. decorus .......................................... 50 3.2.3 Assessing evolutionary mechanisms for variation in hybrid seed inviability . 52 3.2.3.1 Determining ploidy and its effects on hybrid seed inviability .................... 52 3.2.3.1 Assessing potential correlates of hybrid seed inviability ............................. 53 3.2.4 Crossing survey within species ............................................................................... 55 3.2.5 Statistical Analyses .................................................................................................... 56 3.3 Results .............................................................................................................................. 57 3.3.1 Phenotypic and genetic divergence in perennials of the Mimulus guttatus species complex .................................................................................................................. 57 3.3.2 Hybrid seed inviability between M. decorus and M. guttatus .............................. 60 3.3.3 The role of whole genome duplication in hybrid seed inviability between M. decorus and M. guttatus ...................................................................................................... 64 3.3.4 Correlates of hybrid seed inviability ...................................................................... 69 3.3.5 Hybrid seed inviability with M. decorus and M. guttatus ..................................... 72 3.4 Discussion ........................................................................................................................ 77 3.4.1 Phenotypic and genetic diversity with perennials of the M.
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