PUB - Publikationen an der Universität Bielefeld

The forces that maintain stable boundaries between closely related groups are poorly characterized in theFungi. In other organisms prezygotic barriers, such as assortative mating, are sufficient to reinforce local adaptation and prevent hybridization, yet assortative mating and other prezygotic barriers are largely absent in most fungi. Postzygotic barriers, such as large structural changes across the genome, can also maintain lineage segregation through hybrid incompatibility. The role of structural variation in speciation has been well characterized in a wide array of animals and plants, but not in theFungi, where it may be relatively uncommon. Here, we use a pan-genomic approach in the globally distributed ectomycorrhizal fungusBoletus edulisBull. with 310 whole genome sequences and 22 newly generated reference genomes to identify whether large genomic changes are necessary to maintain lineage segregation in the presence of ongoing gene flow. In addition, we evaluate the extent to which different lineages possess unique repertories of saprotrophic and effector gene families to determine whether lineages exhibit distinct ecological capacities that contribute toward lineage segregation. We show thatB. edulispossesses one of the most diverse pan-genomes of eukaryotes, with the lowest proportion of core proteins identified in theFungi. Pan-genomic clustering correlates more with geography than with gene flow or phylogenetic relatedness. We also show that structural variation is abundant withinB. edulis, but is rarely fixed within a lineage or even shared between two individuals. Moreover, we find that a similar degree of genomic synteny exists between genomes of different lineages as between genomes of the same lineage. Functional protein analysis shows that a new lineage ofB. edulisfrom tropical Guatemala has significant contractions in most saprotrophic gene families and possesses a distinct saprotrophic enzyme repertoire. This lineage also a carries a clear signal of a demographic bottleneck, has very low genome-wide heterozygosity, and an inflated genome size, consistent with a substantial shift in ecological niche. In addition, we reveal preliminary evidence for subtle differences in host preference among EuropeanB. edulis. Altogether, our results provide clear evidence that large changes in genome structure or proteome content are not necessary or perhaps even sufficient to maintain long-term lineage fidelity in the presence of ongoing gene flow. Instead, it appears that subtle differences in ecological tendencies can maintain stable boundaries through time.