Mistletoe-Vector-Host Interactions: From Within-Host Processes to Population Genetic Structure

Abstract

The majority of free-living species serve as hosts to multiple parasite and pathogen species, and parasitism is the most frequent interaction type in many food webs. Additionally, diversification rates increase following evolutionary transitions to parasitism. Yet, many aspects of parasite ecology and evolution remain unclear, including how parasites interact within individual hosts, what processes underlie parasite diversification, and how interactions with vectors influence parasite fitness and population dynamics. Parasitic plants provide convenient but underutilized study systems for investigating each of these questions. Entire infections can be characterized and followed in the field over time, and the interactions with vectors can be studied in the framework of pollination and seed dispersal processes. My dissertation concerns host and vector interactions with a geographically widespread, ecologically important parasitic plant, desert mistletoe (Phoradendron californicum), from within host individuals to among host species. I have employed an integrative approach involving experimental (Appendix A) and observational (Appendix B) field ecology, population genetics (Appendix C), and mathematical modeling (Appendix D). At the within-host scale, I show that the size and sex ratio of the infrapopulation (population of one parasite species infecting a single host) independently influence multiple components of parasite fitness through resource competition, within-host mate limitation, and pollen vector attraction (Appendix A). These results, along with genetic structuring at the level of the host individual (Appendix C), indicate that much of mistletoe mating occurs within an infrapopulation. This within-host mating along with differences in flowering phenology and pollinator community composition between mistletoes on velvet mesquite (Prosopis velutina) and other dominant host species (Appendix B) likely contributes to the maintenance of genetically distinct host-associated races that are consistent across space (Appendix C). The genetic and ecological patterns are consistent with the existence of barriers to gene flow between the host races that are asymmetric and stronger at mating (pollination) than at dispersal and establishment (Appendix C). In addition to genetic differences and divergence in many reproductive traits (Appendix B) by host species, the dynamics of parasitic plants may be further complicated by indirect interactions that result from direct interactions between the pollen and seed vectors. Using a simple mathematical model relevant to desert mistletoe and many other mutualistic systems, I find that the persistence and population dynamical outcomes for plants and their partners critically depend on the strength of antagonism between the partners and the degree of specialization of the partners on the mutualistic system (Appendix D). As a whole, this work emphasizes the ecological and evolutionary complexity of parasite-host-vector interactions and the utility of research on parasitic plants for answering fundamental questions in biology.