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Species' distributions and abundances are shifting in response to climate change. Most species harbor microbial symbionts that have the potential to influence these responses. Mutualistic microbial symbionts may provide resilience to environmental change by protecting their hosts from increasing stress. However, environmental change that disrupts these interactions may lead to declines in hosts or symbionts. Microbes preserved within herbarium 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 (Epichloe endophytes), which can protect hosts from abiotic stress, have changed over time in response to climate change, and how these changes vary across host species' ranges. Specifically, we analyzed 2,346 herbarium specimens of three grass host species collected over the last two centuries (1824 -- 2019) for the presence or absence of endophyte symbiosis, and evaluated spatial and temporal trends in endophyte prevalence. We found that endophytes increased in prevalence over the last two centuries from ca. 25% prevalence to ca. 75% prevalence, on average, across three host species. We also found that changes in prevalence were associated with observed changes in seasonal climate drivers; notably increasing precipitation corresponding to each host species' peak growing season and changes in off-peak season variability in precipitation. Our analysis performed favorably in an out-of-sample predictive test with contemporary data, however we identified greater local-scale variability in endophyte prevalence in contemporary data compared to historic data, suggesting that model fusion may be an important step moving forward. Our results provide novel evidence for a cryptic biological response to climate change that may contribute to the resilience of host-microbe symbiosis through context-dependent benefits that confer a fitness advantage to symbiotic hosts under environmental change. 

This project was designed to understand the demographic effects of vertically transmitted fungal endophytes (Epichloë spp.) on their grass hosts. The experiment includes seven host-symbiont taxonomic pairs: Agrostis perennans - E. amarillans, Elymus villosus - E. elymi, Elymus virginicus - E. elymi or EviTG-1, Festuca subverticillata - E. starrii, Poa alsodes - E. alsodes, Poa sylvestris - E. PsyTG-1, Schedonorus arundinaceus - E. coenophiala. Experimental plots were established at the Indiana University Lilly-Dickey Woods Research and Teaching Preserve in south-central Indiana, USA in 2007. For each species, 5-10 plots were planted with naturally symbiotic (S+) hosts, and 5-10 plots were plated with hosts that were disinfected of fungal endophytes by heat treatment (S-). Over 15 years (2007-2022) we collected demographic data on the survival, growth, reproduction, and recruitment of all plants in all plots. Beginning in 2018 we also collected data on the locations of all plants in every plot. 

Abstract Understanding mechanisms that generate range limits is central to knowing why species are found where they are and how they will respond to environmental change. There is growing awareness that biotic interactions play an important role in generating range limits. However, current theory and data overwhelmingly focus on abiotic drivers and antagonistic interactions. Here we explore the effect that mutualists have on their partner's range limits: the geographic “footprint” of mutualism. This footprint arises from two general processes: modification of a partner's niche through environment‐dependent fitness effects and, for a subset of mutualisms, dispersal opportunities that lead suitable habitats to be filled. We developed a conceptual framework that organizes different footprints of mutualism and the underlying mechanisms that shape them, and evaluated supporting empirical evidence from the primary literature. In the available literature, we found that the fitness benefits and dispersal opportunities provided by mutualism can extend species' ranges; conversely, the absence of mutualism can constrain species from otherwise suitable regions of their range. Most studies found that the footprint of mutualism is driven by changes in the frequency of mutualist partners from range core to range edge, whereas fewer found changes in interaction outcomes, the diversity of partners, or varying sensitivities of fitness to the effects of mutualists. We discuss these findings with respect to specialization, dependence, and intimacy of mutualism. Much remains unknown about the geographic footprint of mutualisms, leaving fruitful areas for future work. A particularly important future direction is to explore the role of mutualism during range shifts under global change, including the promotion of shifts at leading edges and persistence at trailing edges.