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TItle: The structure, function, and evolution of the fern vascular system
Abstract: Nearly 425 million years ago land plants evolved novel tissues to move water and sugar more efficiently through their body. These conducting tissues, xylem and phloem, amplified mass flow rates by orders of magnitude, allowing plants to increase their photosynthetic capacity, grow larger, and alter aspects of the terrestrial ecosystem including carbon dioxide modulation and increased oxygenation, in turn, profoundly affecting the course of evolution for life on land.
The three-dimensional arrangement of xylem and phloem within the stem (vascular architecture) is remarkably variable across living and extinct plants. Some of the most impressive displays of this variation occur in the ferns, a diverse clade of land plants with a nearly 400-million- year evolutionary history. Despite over two centuries of study on the vascular system, we still do not know why this diversity exists or how this variation has evolved. Using an arsenal of methodologies, I provide answers to these questions and overturn long held hypotheses on the structure, function, and evolution of the fern vascular system.
First, by integrating high resolution micro-computed tomography, with empirical measurements of leaf water status, I explored how ferns move water through their body. I found that, regardless of broad vascular patterning, nodes (areas of leaf production) are sites of low hydraulic conductivity, while internodes are areas of high conductivity. These nodal chokepoints seem to be associated with drops in distal leaf water status when stems are locally uprooted. Similar nodal chokepoints have previously been documented in woody seed plants, where they are hypothesized to protect the plant from the spread of damage or disease. I suspect that this is also the case in ferns, where nodal chokepoints act as ‘safety-valves’, hydraulically localizing each metameric unit of the plant. Yet, these chokepoints also decrease the amount of water that can freely move across the fern rhizome, decreasing the hydraulic integration of an individual. This suggests that there is a functional tradeoff in the principal construction of the fern body plan.
Furthering this work, I adapted novel optical methods of estimating species vulnerability to drought to determine how the construction of the vascular system in stems affects a species drought tolerance. Overall, I found that stem vulnerability to embolism was correlated most strongly with cellular-level traits, not the overarching three-dimensional architecture of the vascular system. Importantly, I also found that leaves tend to be much more sensitive to drought, meaning leaves fully desiccate before stems reach significant levels of drought stress. These insights suggest that there is no significant correlation between vascular dissection and drought tolerance, and that drought may not be a common stressor on fern rhizomes under current drought regimes.
Finally, by incorporating anatomical data from over 3,300 species with comprehensive phylogenetic comparative methods, I asked how the diversity of vascular architecture has evolved during the 400 million years of fern history. These analyses revealed three major paradigm shifts in our understanding of vascular evolution. 1. Canonical theories on the stepwise and unidirectional evolution of vascular architecture do not capture the complexities of character evolution among ferns. Rather, a new model permitting polymorphic states, increased transitions, rate heterogeneity, and multiple reversions is more likely. 2. Major shifts in vascular architecture correspond to developmental changes in leaf and stem size, not regional water availability. and 3. Rapid bursts of vascular innovation underly early, but not late, fern diversification.
Integrating information gleaned across these three projects, I propose that the immense variation in the three-dimensional construction of the fern vascular system is not a product of direct selection on any optimal pattern. Rather, vascular architecture in ferns reflects the evolution of structural modifications that have been strongly shaped by changes in shoot morphology and body size. These insights overturn long standing canonical hypotheses on the evolution of primary vascular architecture and reveal that the Carboniferous period was a time of rapid structural diversification that then shaped the subsequent history of ferns.
Committee: Ned Friedman (Advisor), Chuck Davis, Gonzalo Giribet, Missy Holbrook (Chair) and Andrew Knoll