Species fundamentally vary in their abundance, spanning a range from federally endangered species to severely weedy invaders. Several hypotheses have been proposed to explain this pattern, but none sufficiently account for observed variation. In part, this failure might reflect the fact that microbial symbioses (widespread, mutually beneficial associations between microbes and plants) have been largely ignored. This proposal forges a new direction by evaluating the role of microbial symbioses in governing rarity and invasiveness. Taking advantage of the experimentally tractable symbioses between grasses and microbial endophytes (fungi that live within plant leaves), proposed experiments and demographic models test whether and how symbionts increase host abundance. In grasses, endophytes may improve host resistance to herbivory through the production of alkaloids toxic to insects and mammals and also may enhance host drought tolerance. Comparative experiments on paired rare and common grass species will test predictions that symbionts benefits are greater for common than rare host species and differ between native and non-native hosts, providing the most comprehensive study to date on the ecology of grass-endophyte symbioses. A clearer understanding of endophyte ecology can offer novel strategies for rare plant conservation and invasive plant control (e.g., via endophyte additions or eliminations). Through networks established in both Indiana and Texas, information will be broadly communicated to state agencies, preserve managers, seed companies, and conservation organizations. The work will additionally integrate teaching and research, by training graduate and undergraduate students as well as bringing contemporary research into the classroom.
Species fundamentally vary in their relative abundance, spanning a range from invasive to rare. Several hypotheses have been proposed to explain this variation, but the literature is replete with conflicting results, and currently proposed mechanisms do not sufficiently account for the observed variation. Investigations of symbiosis may help resolve the lack of consistency in research on rarity, commonness, and invasiveness. Beneficial symbionts can increase host resistance to biotic and abiotic stress and may thereby affect the ecological dominance of host species. This research combined diverse approaches to test two related questions on the ecological impacts of symbiosis. (A) Does symbiosis increase host abundance? (B) Through what mechanisms do symbionts affect host abundance? By drawing comparisons across several host species, including rare, common, and invasive grasses, I have built the most comprehensive study to date on the ecology of grass-endophyte symbioses, with results that generalize to other symbiotic interactions. The systems developed here will be used into the indefinite future for elucidating the ecological consequences of endophyte symbiosis in natural plant populations and for investigating the evolution of symbiosis. Intellectual Merit (A) Does symbiosis increase host abundance? Identifying the mechanisms that control species abundances is a fundamental goal of ecological research. Historically, abiotic factors (resource availability, disturbance) and antagonistic interactions (competition, predation) have been considered the major determinants of abundance. In contrast, symbioses have received little attention, despite their ubiquity and increasingly well-recognized importance in nature. Specifically, few studies have linked the effects of symbionts on individual hosts to effects on host population growth. This work necessitated large-scale and long-term field experiments that manipulated endophyte presence and tracked population dynamics across of several rare, common, and non-native grass hosts. This research has transcended traditional approaches of plant-symbiont research by employing matrix models and integral projection models to predict rates of population growth and by making phylogenetically-controlled comparisons across multiple species. Comparative work has tested predictions that symbionts' benefits are greater for common than rare hosts and differ between native and non-native species. Our results are consistent with the hypothesis that endophyte symbiosis promotes host dominance, and experiments show significant effects of endophytes on host survival, growth, and reproduction. However, we have found stronger influences of host plant evolutionary history than host plant dominance on the strength of ecological benefits of symbiosis. Symbionts contribute an additional, but often overlooked, layer of diversity in ecosystems, and their inclusion in ecological research has helped to increase the realism of both experiments and theory. The development of the systems and species for this project (including disinfection protocols, artificial infection techniques, immunoblot optimizations, germination protocols) constituted a large scale effort to understand endophyte symbiosis across host species. This work has resulted in new protocols for working with foliar fungal endophytes, new collaborations to determine the molecular systematics and alkaloid genes of the endophytes, the largest survey to date of endophyte frequencies in natural grass populations, and novel perspectives on the role of vertical transmission in symbiotic interactions. I have also furthered investigations of the causes and consequences of endophyte symbioses in invasive plants. (B) Through what mechanisms do symbionts affect host abundance? A large body of agricultural literature predicts that endophytes’ benefits to plant hosts occur mainly through the amelioration of biotic (herbivores and pathogens) and abiotic (e.g., drought) stress. The ecological consequences of symbiosis with endophytes were formerly unknown for nearly all native endophyte hosts. This gap in understanding of the ecology of endophytes provided rich opportunities for independent research by undergraduate students. Experiments tested and confirmed several potential mechanisms across diverse host species. resistance and tolerance to drought resistance to herbivores (insect and mammals) improved competitive ability tolerance to shade imperfect endophyte transmission alteration of plant reproductive biology (allocation to seeds vs. pollen) modification of soil microbial communities Broader Impacts This grant has produced 25 publications, 3 manuscripts in preparation for submission, and 16 undergraduate independent research experiences (including REU projects and 10 undergraduate-authored publications), and has contributed to the training of 7 graduate students (2 MS theses) and 3 post-doctoral associates. Funding has resulted in the development of a graduate core course to improve graduate training at Rice University, K-12 teacher education programs in microbial ecology, outreach to high school biology students through on-campus workshops and Citizen Science programs at local schools, and improved understanding of rare plant conservation. Funding has supported training of 44 undergraduates in microbial ecology, including 27 female, 5 Hispanic, and 2 African American students. In addition, 11 technicians, including an underrepresented minority (Hispanic) and 7 other females, have received extensive training in microbial methods and ecological research.
