Increasing Prevalence of Plant-Fungal Symbiosis Across Two Centuries of Environmental Change

Species' distributions and abundances are shifting in response to ongoing global climate change. Mutualistic microbial symbionts can provide hosts with protection from environmental stress that may promote resilience under environmental change; however, this change may also disrupt species interactions and lead to declines in hosts and/or symbionts. Symbionts preserved within natural history specimens offer a unique opportunity to quantify changes in microbial symbiosis across broad temporal and spatial scales. We asked how the prevalence of seed-transmitted fungal symbionts of grasses (Epichloë endophytes) has changed over time in response to climate change, and how these changes vary across host species' distributions. Specifically, we examined 2346 herbarium specimens of three grass host species (Agrostis hyemalis, Agrostis perennans, Elymus virginicus) collected over the past two centuries (1824-2019) for the presence or absence of Epichloë symbiosis. Analysis of an approximate Bayesian spatially varying coefficients model revealed that endophytes increased in prevalence over the last two centuries from ca. 25% to ca. 75% prevalence, on average, across three host species. Changes in seasonal climate drivers were associated with increasing endophyte prevalence. Notably, increasing precipitation during the peak growing season for Agrostis species and decreasing precipitation for E. virginicus were associated with increasing endophyte prevalence. Changes in the variability of precipitation and temperature during off-peak seasons were also important predictors of increasing endophyte prevalence. Our model performed favorably in an out-of-sample predictive test with contemporary survey data from across 63 populations, a rare extra step in collections-based research. However, there was greater local-scale variability in endophyte prevalence in contemporary data compared to model predictions, suggesting new directions that could improve predictive accuracy. Our results provide novel evidence for a cryptic biological response to climate change that may contribute to the resilience of host-microbe symbiosis through fitness benefits to symbiotic hosts.