skip to main content

Title: Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis
Abstract Background and Aims The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? Methods We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. Key Results Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. Conclusions Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.  more » « less
Award ID(s):
1754468 1754433
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Annals of Botany
Page Range / eLocation ID:
981 to 991
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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.

    more » « less
  2. Abstract Aim

    The endophyteEpichloë alsodes, with known insecticidal properties, is found in a majority ofPoa alsodespopulations across a latitudinal gradient from North Carolina to New York. A second endophyte,E. schardliivar.pennsylvanica, with known insect‐deterring effects, is limited to a few populations in Pennsylvania. We explored whether such disparate differences in distributions could be explained by selection from biotic and abiotic environmental factors.


    Along the Appalachian Mountains from North Carolina to New York, USA.




    Studied correlations of infection frequencies with abiotic and biotic environmental factors. Checked endophyte vertical transmission rates and effects on overwintering survival. With artificial inoculations for two host populations with two isolates per endophyte species, tested endophyte–host compatibility. Studied effects of isolates on host performances in greenhouse experiment with four water‐nutrients treatments.


    Correlation analysis revealed positive associations ofE. alsodesfrequency with July Max temperatures, July precipitation, and soil nitrogen and phosphorous and negative associations with insect damage and soil magnesium and potassium. Plants infected withE. alsodeshad increased overwintering survival compared to plants infected withE. schardliior uninfected (E−) plants. Artificial inoculations indicated thatE. alsodeshad better compatibility with a variety of host genotypes than didE. schardlii. The experiment with reciprocally inoculated plants grown under different treatments revealed a complexity of interactions among hosts, endophyte species, isolate within species, host plant origin, and environmental factors. Neither of the endophyte species increased plant biomass, but some of the isolates within each species had other effects on plant growth such as increased root:shoot ratio, number of tillers, and changes in plant height that might affect host fitness.

    Main conclusion

    In the absence of clear and consistent effects of the endophytes on host growth, the differences in endophyte‐mediated protection against herbivores may be the key factor determining distribution differences of the two endophyte species.

    more » « less
  3. Premise

    Microbial symbionts can buffer plant hosts from environmental change. Therefore, understanding how global change factors alter the associations between hosts and their microbial symbionts may improve predictions of future changes in host population dynamics and microbial diversity. Here, we investigated how one global change factor, precipitation, affected the maintenance or loss of symbiotic fungal endophytes in a C3grass host. Specifically, we examined the distinct responses ofEpichloë(vertically transmitted and systemic) and non‐epichloid endophytes (typically horizontally transmitted and localized) by considering (1) how precipitation altered associations withEpichloëand non‐epichloid endophytic taxa across host ontogeny, and (2) interactive effects of water availability andEpichloëon early seedling life history stages.


    We manipulated the presence ofEpichloë amarillansin American beachgrass (Ammophila breviligulata) in a multiyear field experiment that imposed three precipitation regimes (ambient or ±30% rainfall). In laboratory assays, we investigated the interactive effects of water availability andEpichloëon seed viability and germination.


    Reduced precipitation decreased the incidence ofEpichloëin leaves in the final sampling period, but had no effect on associations with non‐epichloid taxa.Epichloëreduced the incidence of non‐epichloid endophytes, including systemic p‐endophytes, in seeds. Laboratory assays suggested that association withEpichloëis likely maintained, in part, due to increased seed viability and germination regardless of water availability.


    Our study empirically demonstrates several pathways for plant symbionts to be lost or maintained across host ontogeny and suggests that reductions in precipitation can drive the loss of a plant's microbial symbionts.

    more » « less
  4. Abstract

    Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect–bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host–symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.

    more » « less
  5. Plants are typically infected by a consortium of internal fungal associates, including endophytes in their leaves, as well as arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE) in their roots. It is logical that these organisms will interact with each other and the abiotic environment in addition to their host, but there has been little work to date examining the interactions of multiple symbionts within single plant hosts, or how the relationships among symbionts and their host change across environmental conditions. We examined the grassAgrostis capillarisin the context of a climate manipulation experiment in prairies in the Pacific Northwest, USA. Each plant was tested for presence of foliar endophytes in the genusEpichloë, and we measured percent root length colonized (PRLC) by AMF and DSE. We hypothesized that the symbionts in our system would be in competition for host resources, that the outcome of that competition could be driven by the benefit to the host, and that the host plants would be able to allocate carbon to the symbionts in such a way as to maximize fitness benefit within a particular environmental context. We found a correlation between DSE and AMF PRLC across climatic conditions; we also found a fitness cost to increasing DSE colonization, which was negated by presence ofEpichloëendophytes. These results suggest that selective pressure on the host is likely to favor host/symbiont relationships that structure the community of symbionts in the most beneficial way possible for the host, not necessarily favoring the individual symbiont that is most beneficial to the host in isolation. These results highlight the need for a more integrative, systems approach to the study of host/symbiont consortia.

    more » « less