Gene genealogies reveal cryptic species and host preferences for the pine fungal pathogenGrosmannia clavigera

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Abstract
Grosmannia clavigerais a fungal pathogen of pine forests in western North America and a symbiotic associate of two sister bark beetles:Dendroctonus ponderosaeandD. jeffreyi. This fungus and its beetle associateD. ponderosaeare expanding in large epidemics in western North America. Using the fungal genome sequence and gene annotations, we assessed whether fungal isolates from the two beetles inhabiting different species of pine in epidemic regions of western Canada and the USA, as well as in localized populations outside of the current epidemic, represent different genetic lineages. We characterized nucleotide variations in 67 genomic regions and selected 15 for the phylogenetic analysis. Using concordance of gene genealogies and distinct ecological characteristics, we identified two sibling phylogenetic species: Gc and Gs. Where the closely relatedPinus ponderosaandP. jeffreyiare infested by localized populations of their respective beetles, Gc is present. In contrast, Gs is an exclusive associate ofD. ponderosaemainly present on its primary host‐treeP. contorta; however, in the current epidemic areas, it is also found in other pine species. These results suggest that the host‐tree species and the beetle population dynamics may be important factors associated with the genetic divergence and diversity of fungal partners in the beetle‐tree ecosystems. Gc represents the originalG. clavigeraholotype, and Gs should be described as a new species.