Foliar pathogens of Populus angustifolia are consistent with a hypothesis of Beringian migration into North America

Populus angustifolia, the narrowleaf cottonwood, is considered one of two native species of Populus section Tacamahaca restricted to western North America. Efforts to construct a definitive phylogeny of Populus spp. are complicated by ancient hybridization, but some phylogenetic analyses suggest P. angustifolia is more closely related to Asian congeners than to Populus trichocarpa, the other species of Populus section Tacamahaca in western North America. Because hosts and their obligate symbionts can display parallel phylogeographic patterns, we evaluated the possibility of a Beringian migration into North America by an Asian ancestor of P. angustifolia by determining the distributions, host preferences, and, in some cases, closest phylogenetic relatives of fungal leaf pathogens of P. angustifolia. Phyllactinia populi, a common foliar pathogen on Populus spp. in Asia but unknown on P. trichocarpa, was found on P. angustifolia in multiple sites. Mycosphaerella angustifoliorum, also unknown on P. trichocarpa, was commonly collected on P. angustifolia. Conversely, many common foliar pathogens of P. trichocarpa in western North America were not found on P. angustifolia; only Melampsora×columbiana and Drepanopeziza populi were common to both Populus species. Phylogenetic analyses revealed that M. angustifoliorum was not part of the diversification of Mycosphaerella on Populus that includes all other Mycosphaerella species on Populus in North America: Mycosphaerella populicola, Mycosphaerella populorum, M. sp. 1, and M. sp. 2. The latter two undescribed species represent a newly discovered diversification of M. populorum in western North America. Overall, the leaf pathogen community of P. angustifolia is consistent with a Beringian migration into North America by the ancestor of P. angustifolia.

► Our study integrates fungal parasites into a study of long-term host migration history.
► Ours is the first comprehensive study of the fungal pathogens of Populus angustifolia.
► We found evidence of Mycosphaerella populorum diversification in western North America.
► Populus angustifolia pathogens are consistent with a Beringian migration into North America.