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UNIVERSITY OF CALIFORNIA SANTA CRUZ ADAPTIVE DIVERGENCE AND SPECIATION IN THE CALIFORNIA SERPENTINE FLORA A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Shelley A. Sianta September 2019 The Dissertation of Shelley A. Sianta is approved: ________________________________ Professor Kathleen M. Kay, Chair ________________________________ Professor Ingrid M. Parker ________________________________ Professor Beth Shapiro ________________________________ Professor Sharon Y. Strauss ________________________________ Professor Nishanta Rajakaruna ________________________________ Quentin Williams Acting Vice Provost and Dean of Graduate Studies Copyright Ó by Shelley A. Sianta 2015 TABLE OF CONTENTS Page List of Tables and Figures v Abstract viii Acknowledgements xi Statement of contribution xv General Introduction 1 Bibliography………………………………………………...13 Chapter 1: Adaptation and divergence in edaphic specialists and generalists: serpentine soil endemics in the California flora occur in barer serpentine habitats with lower soil calcium levels than serpentine tolerators 18 Bibliography………………………………………………...53 Tables……………………………….……………….............63 Figures………………………………………………............65 Appendix…………………………………………................70 Chapter 2: Across the speciation continuum: genetically-based flowering time shifts evolve early in speciation following adaptation to serpentine soils 79 Bibliography………………………………………………...113 Tables………………………………………………..............121 Figures………………………………………………............127 iii Chapter 3: Trade-offs between serpentine adaptation and competitive ability are associated with the evolution of serpentine endemic species but not through habitat isolation 137 Bibliography……………………………………….………...171 Tables……………………….……………………….............177 Figures…………………………….…………………............182 Appendix…...……….……..…………………………............191 Chapter 4: Phylogenomic analysis resolves a controversial case of putative progenitor-derivative speciation for the serpentine endemic Clarkia franciscana 193 Bibliography………………………………………………...216 Tables…………………………………………….….............223 Figures………………………………………………............224 Synthesis 234 Bibliography………………………………………………...245 iv LIST OF FIGURES AND TABLES Page Table 1.1 Description of taxa used in study 63 Table 1.2 Effect of pair type on soil harshness variables 64 Figure 1.1 Conceptual diagram of experimental design 65 Figure 1.2 Difference in soil harshness between serpentine taxa 66 Figure 1.3 Difference in bare ground between serpentine taxa 67 Figure 1.4 Pairwise divergence in multivariate soil environment 68 Figure 1.5 Pairwise divergence in bare ground 69 Table 2.1 Taxa used in this study 121 Table 2.2 Pairwise difference in flowering onset 122 Table 2.3 Plastic vs genetic effects on flowering onset 123 Table 2.4 Pairwise differences in maternal family flowering time reaction norms 124 Table 2.5 Phenotypic selection on flowering onset in serpentine soil 126 Figure 2.1 Conceptual diagram of interaction of seed dispersal, plasticity and reproductive isolation 127 Figure 2.2 Flowering onset shifts among all sister taxa pairs 128 Figure 2.3 Characterization of plastic vs genetic differentiation in flowering time shifts 129 Figure 2.4 Boxplots of flowering onset between three treatments 130 Figure 2.5 Maternal family reaction norms in flowering onset 131 Figure 2.6 Phenotypic selection on flowering time in serpentine soil 132 Figure 2.7 Phenological isolation in two ecological contexts 133 Figure 2.8 Effect of multivariate soil divergence on flowering shifts 134 v Figure 2.9 Effect of climate divergence on flowering shifts 135 Figure 2.10 Box plots of flowering onset showing patterns of genetic assimilation and compensation 136 Table 3.1 Table of taxa used in this study 177 Table 3.2 Summary of fitness trade-offs 179 Table 3.3 Summary of habitat isolation 181 Figure 3.1 Conceptual diagram of fitness contrasts 182 Figure 3.2 Fitness trade-offs of nonserpentine taxa in serpentine soil 183 Figure 3.3 Habitat isolation in serpentine soil 184 Figure 3.4 Fitness trade-offs of serpentine taxa in nonserpentine soil 185 Figure 3.5 Habitat isolation in nonserpentine soil 186 Figure 3.6 Fitness trade-offs of serpentine taxa in competitive nonserpentine soil 187 Figure 3.7 Habitat isolation in competitive nonserpentine soil 188 Figure 3.8 Competitive ability of serpentine taxa 189 Figure 3.9 Pairwise divergence in competitive ability 190 Table 4.1 Population-level samples used in this study 223 Figure 4.1 Geographic ranges and sampling locations of samples 224 Figure 4.2 ASTRAL species tree 225 Figure 4.3 RAxML supermatrix tree without outliers 226 Figure 4.4 ASTRAL tree with showing gene tree discordance 227 Figure 4.S1 RAxML tree with outliers 228 Figure 4.S2 Single Lite Log Likelihood outlier test 229 vi Figure 4.S3 RAxML gene tree of gene AT4G29490 230 Figure 4.S4 RAxML gene tree of gene AT5G02250 231 Figure 4.S5 RAxML gene tree of gene AT5G03905 232 Figure 4.S6 RAxML gene tree of gene AT5G50930 233 vii ABSTRACT Adaptive divergence and speciation in the California serpentine flora Shelley A. Sianta Charles Darwin and Alfred Russel Wallace emphasized the role of adaptive divergence among populations in initiating speciation, and studying the ways in which natural selection causes reproductive isolation among populations is an active field of research. Yet local adaptation to different environments does not always lead to speciation, as evidenced by species occupying a broad range of habitats. The overall goal of this dissertation research was to improve our understanding of how speciation occurs following adaptive divergence, and why it sometimes does not. My study system was the flora associated with naturally- toxic serpentine soils in California, wherein divergence across soil boundaries is accompanied by strong selection, leading to the evolution of both ecologically- variable species (serpentine tolerators) and the evolution of new, ecologically- specialized species (serpentine endemics). I use an experimental comparative design and a population-level phylogenomic approach to understand factors that promote speciation via adaptive divergence in this system. In my first chapter, I tested the hypothesis that serpentine endemics adapt to more harsh serpentine habitats or more divergent habitats relative to their progenitor populations than serpentine tolerators. I quantified soil chemistry data and the percent of bare ground in the habitats of 8 serpentine endemic species, 9 serpentine tolerator species, and in a paired nonserpentine taxon for each of the 17 serpentine species. viii I found that serpentine endemics occur in barer serpentine habitats with lower soil calcium levels than serpentine tolerators. There was no difference in the degree of habitat divergence between tolerator serpentine-nonserpentine pairs and endemic serpentine-nonserpentine pairs. In my second and third chapters, I set up a multi- year greenhouse reciprocal transplant experiment with all 17 serpentine- nonserpentine sister taxa pairs using field-collected seed and soil. I included an additional treatment where I grew members of each taxa pair in the pair’s nonserpentine soil with a standardized competitor, in order to measure the competitive ability of serpentine endemics vs. tolerators. In my second chapter, I quantified timing to first flower and phenological isolation in all pairs to answer the question of whether plasticity in flowering time shifts promotes or constrains speciation. I found that endemic and tolerator sister taxa pairs did not differ in the magnitude of phenological isolation, nor in the degree to which flowering time shifts were plastic versus genetically-based, suggesting that phenological isolation evolves early in the speciation process. Instead the magnitude of flowering time shifts between paired serpentine and nonserpentine sisters were partially explained by how different the pair’s soils were. In my third chapter, I quantified fitness trade-offs, habitat isolation and competitive ability of all pairs to test Arthur Kruckeberg’s long-standing hypothesis that a trade-off between serpentine adaptation and competitive ability promote the evolution of serpentine endemics but not serpentine tolerators. I found that, indeed, serpentine endemics were on average worse competitors than serpentine tolerators. I also found that there is ix more divergence in competitive ability in endemic pairs than tolerator pairs, suggesting that a greater trade-off between serpentine adaptation and competitive ability has occurred in the endemic lineages. Lastly, I revisited a hypothesized case of budding speciation in the triad of species Clarkia franciscana, C. rubicunda and C. amoena. Clarkia franciscana was hypothesized to be a derivative species of C. rubicunda, as it is a very small-ranged serpentine endemic species, with its range subsumed by the range of the more ecologically-diverse C. rubicunda. I used population-level sampling and phylogenomic techniques to determine if there was evidence for progenitor-derivative speciation in this group. I found that there was not, and instead all three species formed well-supported monophyletic groups. However, there was a lot of gene tree discordance regarding the relationship of the three species, suggesting that they evolved simultaneously and rapidly. Instead of being a recently evolved serpentine endemic, as was hypothesized, C. franciscana was likely once a more widespread