Do Pollinators Drive Divergence? Connecting Floral Phenotypes, Pollinators, and Gene Flow to Understand Floral Trait Divergence in Castilleja

Wenzell, Katherine Elizabeth

doi:https://doi.org/10.21985/n2-gcva-w135

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Do Pollinators Drive Divergence? Connecting Floral Phenotypes, Pollinators, and Gene Flow to Understand Floral Trait Divergence in Castilleja

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Interactions with pollinators are thought to be a major driver of the evolution and diversification of angiosperms, yet questions remain about how pollinators mediate plant divergence at early stages and across entire species distributions. Here, I address this knowledge gap using two study groups in the recently-radiating and florally diverse genus Castilleja, the widespread C. sessiliflora and the more restricted species of the C. purpurea complex (C. purpurea, C. citrina, and C. lindheimeri). Chapter 1 examines how phenotypic and genetic differentiation proceed across landscapes by comparing population-level differentiation in floral phenotype and genetic sequence variation among recently diverged groups to explore patterns of diversification under different scenarios of reproductive isolation. I document that these study groups are characterized by high degrees of floral trait divergence, including both continuous variation across a large geographic range and discrete differences across narrow clines, and that this diversity of floral phenotypes has arisen despite little evidence of molecular genetic differentiation, particularly in the narrowly distributed C. purpurea complex. These findings suggest that strong, recent natural selection may be driving observed patterns of divergence in floral phenotype in this rapidly radiating genus, thus laying the groundwork for investigations into the potential drivers of this divergence. Given the central role of pollinators in interacting with flowers and thus shaping the fitness (selection) and mating patterns (gene flow) of many plants, I expect pollinator interactions to be important in imposing selection and shaping the evolution of floral traits. Thus, Chapter 2 explores whether geographic mosaics of ecological interactions with pollinators may underly patterns of floral divergence, by documenting variation in the assemblages of floral visitors among populations across the ranges of C. sessiliflora and the species of the C. purpurea complex. This work identifies considerable variation across geography and among species in the composition and diversity of floral visitors. This chapter connects this variation in floral visitors to variation in population mean floral trait values as well as to differences in reproductive fitness of populations. Finally, a pollinator exclusion experiment conducted in seven natural populations tested the influence of observed variation in corolla length on reproductive fitness (fruit set) of plants exposed to pollination by nocturnal hawkmoth pollinators, given the expected and well-documented association of long floral tubes with pollination by hawkmoths. My results support the hypothesis that long corollas in C. sessiliflora are associated with increased fruit set in plants exposed to hawkmoth pollinators, suggesting the possibility that this distinctive floral trait may represent an adaptation to a novel pollinator group in the genus Castilleja, providing a possible example of pollinator-mediated evolution of floral traits. Finally, Chapter 3 explores how genetic diversity is partitioned within and among populations across species ranges, as well as how interactions with pollinators (as vectors of plant gene flow via movement of pollen) may shape the population genetics of plants, via their foraging behavior and flight distances. The results of this chapter reveal little genetic structure across the range of C. sessiliflora and across the ranges and among the species of the C. purpurea complex. These groups were found to be characterized by a low degree of genetic differentiation among populations, consistent with a likely recent divergence of species and expected ongoing gene flow. I further found evidence that certain pollinator groups may shape the population genetics of plant species by demonstrating that plant populations experiencing higher proportions of visits from some large-bodied far-flying pollinators (hawkmoths in C. sessiliflora and hummingbirds in the C. purpurea complex) are characterized by lower local population differentiation, suggesting pollinators that may forage greater distances among plant populations may support higher population connectivity of plants by contributing to increased gene flow. Taken together, these chapters integrate phenotypic, ecological, and molecular genetic approaches to characterize how plant species respond to geographic variation in pollinator assemblages. By characterizing how pollinators may impact the floral phenotypes and molecular genetic signatures of plant species, this dissertation advances our understanding of how pollinators shape the evolution of plant species across landscapes.

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