Insect-transmitted plant pathogens threaten crop production and conservation of natural habitat. Despite decades of research aimed at controlling these pathogens in crops, our understanding of vector behavior and ecology and genetic diversity beyond the borders of agriculture is lacking, limiting the efficacy of disease management efforts. This dissertation explores these three factors with regard to the transmission of viruses and fastidious bacterial pathogens by phloem-feeding insects in the suborder Sternorrhyncha. In chapter 1, I report how treating cultivated melon with a synthetic plant hormone analog affects symptom induction by two phylogenetically distant viruses, and how this alteration in symptoms may influence vector behavior in ways that decrease pathogen spread. This work demonstrates the potential utility of disease management tools that mitigate symptom development and disrupt transmission-enhancing vector behaviors, rather than solely controlling vector populations or breeding host plants for resistance. In Chapter 2, I pivot to investigate the ecology and population genetics of the bacterial pathogen Candidatus Liberibacter solanacearum (CLso) and its vector, the potato psyllid (Bactericera cockerelli), in natural plant communities in southern California. I report that CLso and potato psyllids commonly associate with the native perennial Solanum umbelliferum, but these CLso and potato psyllid populations are both genetically distinct from and more diverse than their counterparts in agricultural fields. This suggests that multiple sympatric, but genetically isolated populations of potato psyllid may exist in California, with members of these psyllid populations, and CLso, only rarely moving between crop and wild habitats. In Chapter 3, I tested this hypothesis by sampling potato psyllids from both native and crop plant hosts throughout the state of California. I used restriction enzyme-associated DNA-sequencing (RADseq) to assess genetic connectivity between these psyllid populations and evaluated their CLso infection status, to better understand the importance of different potato psyllid genotypes in spreading CLso. Results of this study greatly improve our understanding of CLso and potato psyllid distribution and genetic diversity in an understudied portion of the country. They confirm that studying plant pathogens and their insect vectors in natural habitats could drastically enhance our ability to forecast and manage future outbreaks of plant disease.

Virus ecology in wild plants is a relatively new field of study that has emerged from disciplines of ecology, entomology, and plant pathology. In this dissertation, I critically review progress in plant virus ecology thus far to identify and address major research gaps, then perform a series of empirical studies to address these deficiencies. My analysis revealed that there is a deficit in research on perennial dicot plants, a weak understanding of the factors shaping virus community composition within and between hosts, and a lack of manipulative studies quantifying impacts of crop viruses on wild plant health. To address these understudied areas, I developed a wild, perennial plant study system consisting of keystone perennial hosts in local Riverside county reserves: Cucurbita foetidissima, C. palmata, and Datura wrightii. In Chapter 1 and Chapter 2, I characterized virus communities in several reserves then employed methods from community ecology to determine the factors that shape the virus communities in hosts, populations, and reserves. In Chapter Three, I determined the origins of the most prevalent aphid-transmitted virus in this system, Cucurbit aphid-borne yellows virus (CABYV). And lastly, in Chapter 4, I used manipulative experiments combined with field observations to quantify CABYV effects on cucurbit performance and evaluate how virus infection modifies host interactions with a key aphid vector, Aphis gossypii. Overall, I found that crop-associated viruses are prevalent in the perennial target hosts, which often support multiple infections. Differences between hosts and reserves structure cucurbit virus communities, with some viruses emerging as keystone species. One of these species, CABYV, negatively affects its wild hosts in ways that are relevant for both virus and host persistence within the community.