Eco-evolutionary Drivers of Symbiotic Network Assembly: A Case Study with Cyanolichens

Abstract

Symbiotic interactions, including parasitism, commensalism, and mutualism, form complex networks that are omnipresent in nature. As such, they have played a critical, yet often overlooked, role in the evolution of species across the tree of life. It is only through a better understanding of the mechanisms driving their assembly that we can gain insights into how symbioses have shaped species evolution, diversification, and ecology. The overarching goal of my dissertation research was to determine how symbiotic networks are shaped by evolution and environmental gradients at different scales, from biomes to molecules. I approached this using cyanolichens—a symbiosis between a fungus and a cyanobacteria—as a model system. This dissertation is structured into five research chapters with three major goals: (1) Develop a multi-locus phylogenetic framework for Nostoc cyanobacteria that allows delimitation of meaningful evolutionary units for eco-evolutionary studies; (2) Study the effect of spatial gradients and Nostoc availability on the interaction network of the Peltigera-Nostoc lichen symbiosis; and (3) Identify molecular mechanisms and biomolecules with a potential role in the establishment and maintenance of the Peltigera-Nostoc symbiosis. In Chapter 2, I present a phylogenomic framework for the order Nostocales, which includes Nostoc, and demonstrate that an ancient rapid radiation is the main source of rampant phylogenetic conflict among phylogenies inferred with concatenated datasets. In Chapter 3, I present a phylogenomic framework for the genus Nostoc, which revealed 8 rapid radiations that were associated with the evolution of major plant lineages and with heterogeneous species boundaries across Nostoc. The results from Chapters 2 and 3 suggest that rapid radiations have been a major but neglected force shaping the evolutionary history of cyanobacteria, which challenges long-held practices typically used to infer phylogenies and delimit species for Bacteria. In Chapter 4, I developed a new specialization index that integrates phylogenetic and partner availability. When we applied this index to interaction datasets from several bipartite systems, we found evidence that partner availability is an important driver of specialization patterns, including in cyanolichens from the genus Peltigera. In Chapter 5, we used a large-scale sampling of Peltigera cyanolichens across the province of Alberta, Canada, to understand the spatial pairing mechanisms in the Peltigera-Nostoc symbiosis. This showed that symbiotic pairing is largely driven by the effect of environmental variation on symbiont cooccurrence. Finally, in Chapter 6, we used comparative genomics and a metatranscriptomic experiment to determine the molecular changes that enable Nostoc’s metabolic role (i.e., providing carbon and nitrogen) in the symbiosis with Peltigera.