Human migrations over many centuries have resulted in considerable movements of organisms beyond their natural ranges. Study of these exotic introductions can help us to understand their ecology and biology as well as provide clues for the management of biological invasions. Suillus luteus is one of the most abundant globally introduced symbiotic fungi associated with exotic pine afforestation. I studied the population genomics of native and introduced populations of this ectomycorrhizal fungus to understand its evolution and genetics. Whole genomes of 274 S. luteus strains along with strains of closely related sister species were sequenced using the Illumina sequencing platform. These strains represent native populations of S. luteus from its native range across Europe and Asia as well as from five introduced populations in North America, South America, Australia, New Zealand, and Africa. Taking advantage of this rich dataset, I analyzed and compared the genetic relationships, population genetic parameters, and signatures of selection across populations to understand the natural history of S. luteus, the processes of its introductions, and the evolutionary consequences in the introduced populations.
Using the sister species S. brunnescens as an outgroup, phylogenomic, multi-species coalescent model, and admixture analyses of SNP data revealed three genetically divergent clades from Central Europe, Northern Europe and Asia, which likely represent at least two cryptic species within the single morphological species S. luteus. Phylogenomic analyses showed that all introduced populations belong to the Central Europe clade, and multiple independent introductions for exotic populations in Australia, New Zealand, South America and Africa, and North America. North American introduced populations were found to be the least differentiated from the Central Europe population, implying a more recent introduction and/or limited sexual reproduction since the introduction. The introduced population from South America was the most isolated from others, with little evidence of gene flow with other populations. All introduced populations experienced different levels of loss in genetic diversity and had more limited numbers of mating types, which suggests those exotic population experienced genetic bottlenecks during introduction. Demographic analyses revealed significant expansion of population size for introduced populations in Western Australia and Argentina. Higher inbreeding coefficients were observed in all introduced populations, likely as a result of smaller founder population sizes. However, little evidence for selfing was observed that the mating system of S. luteus still remained high rates of outcrossing in the introduced populations. I examined the occurrence of local adaptation in each population by scanning genome regions of high divergence and selective sweeps. Several genomic regions associated with regulatory functions were observed to have shared signatures of selections among multiple introduced populations, implying their important roles in adaptation for diverse exotic environments.
The genomics approach used to study the mating type loci of S. luteus was applied to genomes of other Suillus and Rhizopogon species to better understand the evolution of the self-incompatibility system in suilloid fungi. I employed a novel method of de novo assembly to assemble the highly divergent self-incompatibility loci and then recovered haplotypes from the genomes. Strong patterns of trans-specific polymorphisms and high sequence divergence in the HD MAT locus suggest that this locus is under strong balancing selection and confirm that this locus functions to control mating types in suilloid fungi. Phylogenetic analyses of HD MAT haplotypes showed that HD MAT loci were multiallelic and that the origins of some mating types predated the split between Rhizopogon and Suillus.
Population genomics of native and introduced populations provides new insight into the evolution of S. luteus, the process and consequences of introduction, and evolution associated with global exotic introductions. This study also demonstrates how the genomics and theories of molecular evolution can be used to study the evolution and genetics of fungi albeit the difficulty in ecological survey and limited genetic methods in ectomycorrhizal fungi.