Biogeographic plant-microbe patterns and process: natural and anthropogenic impacts across three spatial scales

Abstract

The plant microbiome is essential to the maintenance of plant community structure and diversity. In addition, anthropogenic forces are altering these long-standing relationships. Despite the importance of the plant microbiome and increasing human impacts, questions about how the plant microbiome drives plant biogeography and how these microbes and plant-microbe relationships change in response to anthropogenic forces remain understudied. Here, I aim to clarify the microbial contribution to biogeographical patterns of plants, biogeographical patterns of plant-associated microbes themselves, and the nature of the plant-microbe relationship, with patterns and processes contrasted in native systems and in those altered by anthropogenic impacts. The specific aims are to (1) clarify how ubiquitous plant symbionts - mycorrhizal fungi - influence global island biogeographical patterns, as well as subsequent shifts in these patterns due to plant naturalizations, (2) determine how different mycorrhizal types with varying life-history traits may differentially contribute to these patterns, (3) describe the response of plant pathogens to climate and land use impacts using a natural Midwestern precipitation and temperature gradient, and (4) investigate the evolution of the plant-mycorrhizal relationship in native plant species as a result of novel plant-mycorrhizal interactions in Kansas. Together, this work contributes to our understanding of plant-microbe associations across different scales in native systems as well as the consequences of anthropogenic impacts, with implications for conservation and management. Chapter 1 addresses how the limited dispersal of mycorrhizal fungi on oceanic islands act as a colonization filter for plants. This hypothesis was tested using global-scale analyses of ~1.4 million plant occurrences including ~200,000 plant species across ~1100 regions. The results support the operation of a mycorrhizal filter (i.e. the filtering out of mycorrhizal plants on islands), with mycorrhizal associations less common among native island plants than native mainland plants. In addition, the proportion of native mycorrhizal plants in island floras decreased with isolation from mainlands, consistent with a decline in symbiont establishment. Mycorrhizal plants are also shown to contribute disproportionately to the classic latitudinal gradient of plant species diversity, with the proportion of mycorrhizal plants being highest in lower latitudes and decreasing towards higher latitudes. Anthropogenic pressure and land use alter these plant biogeographic patterns, as naturalized floras showed a greater proportion of mycorrhizal plant species on islands than in mainland regions, as expected from anthropogenic co-introduction of plants with their symbionts to islands and anthropogenic disturbance of symbionts in mainland regions. Overall, this work identifies the mycorrhizal association as an overlooked driver of global plant biogeographic patterns with implications for contemporary island biogeography and our understanding of plant invasions. Chapter 2 expands on Chapter 1 by analyzing biogeographical patterns of plants associating with three major types of mycorrhizal fungi. Plant colonization of islands may be limited by the availability of arbuscular mycorrhizal (AM) fungi in particular, which have limited dispersal ability compared to ectomycorrhizal (EM) and orchid mycorrhizal (OM) fungi. We tested for such differential island colonization within contemporary floras worldwide. We found evidence that AM plants experience a stronger mycorrhizal filter than other mycorrhizal or non-mycorrhizal (NM) plants, with decreased proportions of native AM plant species on islands relative to mainlands. This effect intensified with island isolation, particularly for non-endemic plant species. The proportion of endemic AM plant species increased with island isolation, consistent with diversification filling niches left open by the mycorrhizal filter. Naturalized floras featured higher proportions of AM plant species than native floras, a pattern that increased with increasing isolation and land-use intensity. This work provides evidence that the biology of fungal symbionts shapes plant colonization of islands, subsequent diversification and anthropogenic impacts. Chapter 3 uses a natural precipitation and temperature gradient across the Midwestern United States (regional scale) to examine soil-borne pathogen response to climate and land use. Soil-borne pathogens structure plant communities, shaping their diversity, and through these effects may mediate plant responses to climate change and disturbance. Little is known, however, about the environmental determinants of plant pathogen communities. Therefore, this work explored the impact of climate gradients and anthropogenic disturbance on root-associated pathogens – fungal pathogens and oomycetes – in grasslands. In undisturbed grasslands, precipitation and temperature gradients were important predictors of pathogen community richness and composition. Oomycete richness increased with precipitation, while fungal pathogen richness depended on an interaction of precipitation and temperature, with precipitation increasing richness most with higher temperatures. Disturbance altered plant pathogen composition and precipitation and temperature had a reduced effect on pathogen richness and composition in disturbed grasslands. Because pathogens can mediate plant community diversity and structure, the sensitivity of pathogens to disturbance and climate suggests that degradation of the pathogen community may mediate loss, or limit restoration of, native plant diversity in disturbed grasslands, and may modify plant community response to climate change. Chapter 4 focuses on the evolution of the plant-AM fungal relationship at a local scale, to highlight changes to the relationship in novel environments. Arbuscular mycorrhizal fungi (AMF) play an essential role in structuring plant communities, especially in native systems. Nonetheless, increasing anthropogenic disturbance will lead to novel plant-AMF interactions, altering a longstanding co-evolutionary trajectory between plants and their associated AMF. Although emerging work shows that plant-AMF response can evolve over short time scales due to anthropogenic change, little work has evaluated how plant AMF response specificity may evolve due to novel interactions. Therefore, changes in plant-AMF interactions in novel grassland systems were examined by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post-agricultural grasslands to inoculation with both native prairie AMF and non-native AMF. Across four plant species, results support evolution of mycorrhizal response specificity consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post-agricultural populations responding most to non-native AMF. Evolution of mycorrhizal response in two of the four plant species was also found, as overall responsiveness to AMF changed from native to post-agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post-agricultural populations. These results highlight that widespread anthropogenic disturbance can have unintended impacts on the genetic propensities of native plant species’ association with AMF, causing rapid evolutionary change in the benefit native plant species gain from native symbioses. Accumulating evidence supports the important role of the plant microbiome in mediating plant community structure and diversity, yet many basic questions about how the plant microbiome drives plant biogeography and how these microbes may indirectly affect plant communities through anthropogenic change remain understudied. The work in this thesis leveraged global datasets, molecular tools, and greenhouse experiments to begin to answer such questions, contributing substantially to our understanding of two major plant-associated microbes – mutualists and pathogens – at different scales in both native and anthropogenically-altered systems. Together, the research in this thesis improves our understanding of how plant-associated microbes influence plant distribution (biogeography), how climate influences these plant-associated microbes, and the consequences of anthropogenic forces – including land use change, plant introduction, and novel environments – on these patterns and processes.