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1. Context‐dependent variability in the population prevalence and individual fitness effects of plant–fungal symbiosis

   https://doi.org/10.1111/1365-2745.13510  

   Donald, Marion L.; Bohner, Teresa F.; Kolis, Kory M.; Shadow, R. Alan; Rudgers, Jennifer A.; Miller, Tom E. X.; Wilson, ed., G. (November 2020, Journal of Ecology)

   Abstract Heritable symbionts are often observed at intermediate prevalence within host populations, despite expectations that positive fitness feedbacks should drive beneficial symbionts to fixation. Intermediate prevalence may reflect neutral dynamics of symbionts with weak fitness effects, transient dynamics of symbionts trending towards fixation (or elimination), or a stable intermediate outcome determined by the balance of fitness effects and failed symbiont transmission. Theory suggests that these outcomes should depend on symbiont‐conferred demographic effects and vertical transmission efficiency, which may both depend on environmental context.We established experimental populations of winter bent grassAgrostis hyemalisacross a range of prevalence of the heritable fungal endophyteEpichloë amarillans. Using irrigation, we elevated the precipitation for half of the populations, which we hypothesized would weaken the benefits of symbiosis. Across two annual transitions, we assayed 5,485 individuals to determine prevalence and censused 954 individuals for demographic (survival, flowering, reproduction and recruitment) and vertical transmission data. We used hierarchical Bayesian models to infer long‐run equilibria from short‐term changes in symbiont prevalence and estimated demographic vital rates to link individual‐level effects to population‐level outcomes.We found evidence for all three proposed mechanisms for intermediate symbiont prevalence, but the outcome differed qualitatively across years and precipitation treatments. In the first year, symbionts trended towards fixation under drought conditions but drifted neutrally under elevated precipitation. Fixation likely arose from symbiont‐conferred recruitment benefits outweighing reproductive costs under the drought conditions, while elevated precipitation tempered these effects. In the second transition year, we inferred stable intermediate prevalence across both precipitation treatments, which indicated a balance between symbiont conferred recruitment benefits that allowed low‐prevalence populations to increase and imperfect transmission that caused high‐prevalence populations to decrease.Synthesis. We find support for neutral, transient and stable mechanisms underlying symbiont prevalence, indicating that symbiont prevalence is often pushed and pulled in different directions by the composite outcome of symbiont effects on demographic rates and transmission efficiency, and the way in which these processes respond to environmental context. 

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2. Heritable viral symbionts in the family Iflaviridae are widespread among aphids

   https://doi.org/10.1101/2025.02.03.636351  

   Rozo-Lopez, Paula; Torres, Vanesa; Torres, Joseph; Käfer, Simon; Parker, Benjamin J (February 2025, bioRxiv)

   A<sc>bstract</sc> Heritable microbes shape host phenotypes and are important drivers of evolution. While interactions between insects and bacterial symbionts have been extensively studied, the prevalence and consequences of insect-viral symbiosis are an open question. We show that viral symbionts in the familyIflaviridaeare widespread among aphids, an important model for research on bacterial symbiosis. We discovered multiple new species of iflaviruses that are maintained in asexual lines without apparent fitness costs and are transmitted vertically from mothers to offspring. Using field data and phylogenetic evidence, we further show that aphid iflaviruses likely move horizontally across species, but through laboratory experiments, we demonstrated that horizontal transfer among species infesting the same host plants does not persist throughout clonal lineages. Using quantitative PCR and immunohistochemistry, we discovered that viral infections localize in the host fat bodies and developing embryos. Surprisingly, we also found viral infections inside bacteria-housing cells called bacteriocytes, with a positive correlation between viral and bacterial symbiont density, indicating a mechanism for vertical transmission. Together, our work suggests that iflaviruses are an important but previously unrecognized piece of aphid symbiosis and sets the stage to use this model to answer new questions about host-microbe associations. I<sc>mportance</sc>In recent years, the rise of metatranscriptome sequencing has led to the rapid discovery of novel viral sequences in insects. However, few studies have carefully investigated the dynamics of insect-virus interactions to produce a general understanding of viral symbiosis. Aphids are a significant agricultural pest but also an important model for understanding the evolution of host-microbe interactions and the molecular basis of bacterial symbiosis. We show that heritable iflaviruses are an important but previously unrecognized part of the aphid heritable microbiome, with viral symbionts transmitted alongside bacteria from mothers to offspring, potentially via specialized bacteriocytes that house symbiotic microbes. Our findings have important implications for furthering the understanding of insect-microbe symbiosis and the potential for biocontrol of agriculturally relevant pest species. 

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3. Demographic data from long-term symbiont removal experiments with grasses and Epichloë fungal endophytes

   https://doi.org/10.6073/pasta/ea7db07a578fb030a173f37f76596b62  

   Miller, Tom EX; Fowler, Joshua C; Ziegler, Shaun M; Rudgers, Jennifer A; Whitney, Kenneth D; Sheehan, Mark (January 2023, Environmental Data Initiative)

   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. 

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4. How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity

   https://doi.org/10.1093/jeb/voae127  

   Brown, Alexandra L; Koskella, Britt; Boots, Mike (January 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)

   Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

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5. Microbial symbionts buffer hosts from the demographic costs of environmental stochasticity

   https://doi.org/10.1111/ele.14438  

   Fowler, Joshua_C; Ziegler, Shaun; Whitney, Kenneth_D; Rudgers, Jennifer_A; Miller, Tom_E_X (May 2024, Ecology Letters)

   Abstract Species' persistence in increasingly variable climates will depend on resilience against the fitness costs of environmental stochasticity. Most organisms host microbiota that shield against stressors. Here, we test the hypothesis that, by limiting exposure to temporally variable stressors, microbial symbionts reduce hosts' demographic variance. We parameterized stochastic population models using data from a 14‐year symbiont‐removal experiment including seven grass species that hostEpichloëfungal endophytes. Results provide novel evidence that symbiotic benefits arise not only through improved mean fitness, but also through dampened inter‐annual variance. Hosts with “fast” life‐history traits benefited most from symbiont‐mediated demographic buffering. Under current climate conditions, contributions of demographic buffering were modest compared to benefits to mean fitness. However, simulations of increased stochasticity amplified benefits of demographic buffering and made it the more important pathway of host–symbiont mutualism. Microbial‐mediated variance buffering is likely an important, yet cryptic, mechanism of resilience in an increasingly variable world. 

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