Adaptive Divergence and Speciation in the California Serpentine Flora

Author(s): Sianta, Shelley Ann | Advisor(s): Kay, Kathleen M | Abstract: 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. 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 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 species that became restricted to serpentine over time. Taken together, the results from this dissertation are a unique insight into factors that promote progress towards speciation - from the establishment of edaphic ecotypes to the evolution of edaphic endemics.