Symbiosis in the Pacific Ring of Fire : evolutionary-biology of Rhizopogon subgenus Villosuli as mutualists of Pseudotsuga Public Deposited

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  • Rhizopogon is a large genus of ectomycorrhizal (EM) fungi that grows in association with host trees of the family Pinaceae. We have conducted a series of studies investigating the ecology and evolutionary biology of the EM symbiosis shared between R. subgenus Villosuli and trees of the genus Pseudotsuga. Two members of R. subgenus Villosuli, the sister taxa R. vinicolor and R. vesiculosus, are the primary focus of the first two investigations presented in this dissertation. These two species share a sympatric range in the Pacific Northwest where they share a host association with Pseudotsuga menziesii (Douglas fir). In Chapter two we perform a series of container plant experiments, which manipulate substrate stratification and competitive conditions, in order to investigate ecological factors influencing vertical resource partitioning between these species. From the findings of this work we conclude that priority effects and substrate heterogeneity allow R. vinicolor to maintain EM root tips colonized during independent mating events in the face of competition from individuals of R. vesiculosus, which compete for root tips through vegetative expansion. The need for high rates of mating in R. vinicolor populations to successfully compete with R. vesiculosus may be driving microevolutionary adaptation in these species and our second investigation seeks to elucidate the genetic mechanisms that underlie this adaptation. In Chapter three we report the draft genomes of R. vinicolor and R. vesiculosus, which were sequenced in order to characterize the structure and gene content of the loci responsible for mating-type recognition in these fungi. The functional traits of mating-type loci can have dramatic effects upon the population structure and adaptability of fungi and we have sought to characterize these loci to better understand the role of mating in competitive interactions between these species. We have found that the differential life history strategies that shape the population structure of R. vinicolor and R. vesiculosus correlate with differential structure of the mating type B-locus between these species. The B-locus is involved in recognition of compatible mates through the production of lipopeptide pheromones and complementary pheromone receptors. R. vinicolor possesses a greater diversity of both pheromones and receptors than R. vesiculosus and this property is likely reinforced by R. vinicolor's need for frequent mating events to compete successfully with R. vesiculosus. The loss of diversity in this genomic region is a derived trait in R. vesiculosus, which competes successfully through vegetative expansion of a few individuals independent of the frequency of mating. Rhizopogon species possess one of the highest rates of host specificity of any EM fungus and we hypothesize that R. subgenus Villosuli has undergone a process of comigration and cospeciation with their Pseudotsuga hosts. Chapter four seeks to test these hypotheses by conducting a genome-scale phylogeographical analysis of Rhizopogon species growing in association with Pseudotsuga species. We have performed a multinational and intercontinental sampling of Rhizopogon species from the Pacific Rim distribution of all Pseudotsuga species and sequenced low coverage genomes of Rhizopogon species from across this range. Phylogenetic analysis of a 1.97 mbp sequence alignment dataset mined from these genomes demonstrates that members of R. subgenus Villosuli have undergone a process of comigration and cospeciation with their Pseudotsuga hosts. Our work presents macroevolutionary evidence that the EM symbiosis between these genera evolved only once between the common ancestor of R. subgenus Villosuli and the common ancestor of Pseudotsuga in Western North America.
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