Imperiled wanderlust lichens in steppe habitats of western North America comprise geographically structured mycobiont lineages and a reversal to sexual reproduction within this asexual clade

Abstract

The northern North American Cordillera is a globally significant center of endemism. In western North America, imperiled arid steppe habitats support a number of unique species, including several endemic lichens. However, processes driving diversification and endemism in this region remain unclear. In this study, we investigate diversity and phylogeography of the threatened wanderlust lichens (mycobiont = Rhizoplaca species) which occur unattached on calcareous soils in steppe habitats in western North America. Wanderlust lichens comprise three species of lichen-forming fungi (LFF) – Rhizoplaca arbuscula, R. haydenii, and R. idahoensis (endangered, IUCN Red List) – which occur in fragmented populations in Idaho and Wyoming, with more limited populations in southeastern Montana and northern Utah. These lichens reproduce almost exclusively via large, asexual vegetative propagules. Here, our aims were to (i) assess the evolutionary origin of this group and identify phylogeographic structure, (ii) infer ancestral geographic distributions for lineages within this clade, and (iii) use species distribution modeling to better understand the distribution of contemporary populations. Using a genome-skimming approach, we generated a 19.1 Mb alignment, spanning ca. half of the complete LFF genome, from specimens collected throughout the entire range of wanderlust lichens. Based on this phylogeny we investigated phylogeographic patterns using RASP. Finally, we used MaxEnt to estimate species distribution models for R. arbuscula and R. haydenii. We inferred a highly structured topology, with clades corresponding to distinct geographic regions and morphologies represented throughout the group’s distribution. We found that R. robusta, a sexually reproducing taxon, is clearly nested within this asexual lineage. Phylogeographic analyses suggest that both dispersal and vicariance played a significant role throughout the evolutionary history of the vagrant Rhizoplaca clade, with most of the dispersal events originating from the Salmon Basin in eastern Idaho – the center of diversity for this group. Despite the fact that wanderlust lichens are dispersal limited due to large, unspecialized vegetative propagules, we inferred multiple dispersal events crossing the Continental Divide. Comparing herbarium records with SDMs suggests that wanderlust lichens don’t fully occupy the areas of highest distribution probability. In fact, documented records often occur in areas predicted to be only marginally suitable. These data suggest a potential mismatch between contemporary habitats outside of the center of diversity in eastern Idaho with the most suitable habitat, adding to the vulnerability of this imperiled complex of endemic lichens.