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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.

Organisms can alter traits plastically in response to the biotic and abiotic environment in ways that potentially increase fitness, however not all plasticity is adaptive. Despite much study, the effects of plasticity on mating systems, species interactions, and responses to novel environments need further exploration. In this dissertation I study plasticity in an annual plant, Clarkia concinna (Onagraceae) by using a combination of greenhouse experiments and field observations and manipulations. In chapter one I investigate the plastic responses of multiple traits in a greenhouse droughting experiment, comparing the adaptive value of plasticity among plants from eight populations that varied widely in precipitation. Surprisingly, none of the measured traits show adaptive plasticity, and less plastic genotypes show a smaller reduction in fitness in the stressful drought treatment. Plants from locations with greater and more variable annual precipitation tend to show less plasticity in response to drought. In chapter two I focus on the causes of plasticity in floral traits and seed production. Hand-pollinating early flowers on a plant reduces total flower number as well as floral longevity in later flowers. This effect is independent of the abiotic resource conditions (water or nutrient availability). While pollen quality (self or outcross) does not affect floral traits, later fruits on plants with early outcrossed flowers have fewer seeds than fruits on plants with a background of selfing. In chapter three I examine the effects of floral display on pollination. Most pollinators were more likely to move pollen between flowers on the same plant when floral display size was large, increasing the deposition of self pollen. However, the predicted pollinator attraction benefit of large displays is absent in this species, even when there are few surrounding plants. Exploring plasticity in one species though the use of multiple techniques promotes a comprehensive understanding of the subject and leads me to propose potentially fruitful avenues of new research.

Why are there so many angiosperm species compared to other plant groups? Why is angiosperm diversity so high in the tropics? Extensive evidence suggests that plant-pollinator interactions is a significant cause of angiosperm diversification. One important mechanism for pollinator-driven speciation is the transition between pollination systems, known as pollination shifts. Pollination shifts may have played a significant role in shaping tropical diversity. However, the promoting ecological factors and evolutionary processes still need to be fully understood. My dissertation focuses on understanding pollination shifts using a tropical plant system (genus Costus; family Costaceae). I studied the Neotropical Costus clade because it exhibits many parallel shifts from orchid bee to hermit hummingbird pollination. Furthermore, bee- and hummingbird-pollinated Costus species are associated with different suites of floral traits. I used various approaches, from field sampling and experimentation, quantitative floral trait analyses, and pollinator quality comparison in hyper-diverse Neotropical ecosystems in Central and South America. I examined how intrinsic (floral traits) and extrinsic (elevation, pollinator assemblage, pollinator quality) factors may drive pollination shifts and how floral traits change during a pollination shift. In chapter one, I analyzed the variation and association between floral traits and pollinator assemblages in Costus guanaiensis var. tarmicus along an elevational gradient. I found substantial divergence in floral traits and pollinator assemblages across the elevational gradient, establishing the necessary preconditions for pollinator-driven floral divergence. An association between floral and bee trait variation suggests adaptation to the local bee fauna along the elevational gradient. In addition, I found floral traits that might work in hummingbird fitting and attraction in the highest sampled site, and hummingbirds composed the pollinator assemblage there. The beginning of a bee-to-hummingbird pollination shift in the highest-studied site was not ruled out. In chapter two, I investigated whether differences in pollinator quality between bees and hummingbirds could promote bee-to-hummingbird pollination shifts. I compared heterospecific and conspecific pollen loads transferred to the flowers' stigma of bee- and hummingbird-pollinated species and assessed the plant-plant pollinator-mediated interactions in bee- and hummingbird- pollinated Neotropical communities. I found that bees and hummingbirds are high-quality pollinators, transferring large conspecific pollen loads but little heterospecific pollen loads to the stigma. Commensalism prevails among the bee-pollinated community, whereas facilitation prevails among the hummingbird-pollinated community. Neither difference in pollen transfer nor the ecological processes driving the bee- and hummingbird-pollinated communities appear to promote bee-to-hummingbird pollination shifts. In chapter three, I investigated the function of floral traits as anti-bee and pro-bird traits in Costus malortieanus. I artificially modified the size, shape and color of C. malortieanus flowers to resemble a hummingbird-pollinated Costus flower. I exposed the modified flowers to orchid bees and hummingbirds in the field. I found evidence for anti-bee floral traits in the Neotropical Costus clade. Overall, my findings contribute to understanding bee-to-hummingbird pollination shifts beyond temperate systems, giving insights into processes of major adaptive shifts that contribute to tropical plant speciation.

The origin and persistence of species is fundamental to the evolution of biological diversity. Species generally arise in new environments through a combination of ecological divergence and spatial isolation. Under this framework, speciation occurs through three main processes: 1) niche expansion, 2) divergent selection, and 3) the accumulation of reproductive isolating mechanisms. In this dissertation, I tested specific hypotheses about the factors governing each of these stages, using a combination of stochastic simulations and field and greenhouse experiments with life history ecotypes of common monkeyflower Mimulus guttatus DC (Phrymaceae). First, I tested the ecological and genetic determinants of colonization success in flowering plants. In particular, I used stochastic simulations to test the effect of mating system plasticity on the persistence and adaptation of colonizing populations in new environments. I found that a shift to a mixed mating strategy facilitated niche expansion by reducing extinction and promoting adaptation under a broad range of colonization scenarios. In my second and third chapters, I examined the causes and consequences of life history divergence among populations of M. guttatus in central California. In chapter two, I used comparative demography to test for local adaptation and selection on life history traits in a common garden experiment in a montane perennial environment. I found that a perennial life history strategy had the highest performance and that selection favored perennial life history traits, although the native montane perennial ecotype was not locally adapted relative to other inland perennial populations. In chapter three, I quantified multiple isolating mechanisms between a focal montane perennial population and ten other populations spanning the range of life history strategies. I found that total reproductive isolation increased linearly with life history divergence between populations. However, total isolation was achieved through a mosaic of reproductive barriers and enhancers which, individually, exhibited non-linear relationships with life history divergence. These non-linear relationships are likely due to the effects of life history and inbreeding on the evolution of specific isolating mechanisms. Taken together, this work highlights the potential for diverse evolutionary, ecological, and demographic forces to interact to determine progress during the early stages of divergence.