Truffles in the sky: The impact of stochastic and deterministic drivers on Rhizopogon communities of the Madrean sky island archipelago

Temperate forests across the globe are migrating as a result of global warming, but little is known about how changes in climate and host geographic distributions will affect the obligate symbionts of these forests. Analysis of past events can provide insight into how these symbionts have responded to previous climatic changes and inform predictions for contemporary and future climate change events. The Madrean Sky Islands Archipelago (MSIA) comprises mountain “islands” whose Pine-Oak forests appear in stark contrast to the surrounding “sea” of Sonoran Desert vegetation. The archipelago formed due to a post-Pleistocene warming climate that resulted in the expansion of the Sonoran Desert and migration of forests to fragmented, higher elevation areas. Rhizopogon (Boletales) consists of obligate ectomycorrhizal (EcM) symbionts that form truffle sporocarps and associate exclusively with Pinaceae. As such, the MSIA-Rhizopogon system represents a natural experiment of how fungal symbionts responded to climatic change and host migration. Rhizopogon was sampled from nine islands at two sites (one Pinus site and one Pseudotsuga site) per island, and diversity was characterized using the ITS rRNA gene determined from both sporocarps and bioassay-based EcM root tips derived from soil samples collected at each site. We described the biodiversity of Rhizopogon within and among sky islands of the MSIA, and tested whether symbiont species richness and community structure were determined by host association, island identity, geographic distance, or some interaction among these factors. Twenty-five OTUs at 99% similarity in the genus Rhizopogon were identified across nine sky islands with a range of 5–15 OTUs per island. While differential host association with Pinus and Pseudotsuga was a significant driver of community composition, our results supported an even stronger island effect. Furthermore, Rhizopogon communities associated with Pinus forest sites were characterized by random phylogenetic structures across sky islands and are not structured by geographic distance. Our results supported a strong isolation effect that involved historical habitat fragmentation of sky islands in response to past climate changes, and that both host association and stochastic processes, e.g., ecological drift, played a role in shaping Rhizopogon communities of the MSIA.