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

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 grass Agrostis hyemalis across a range of prevalence of the heritable fungal endophyte Epichloë 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.

The geographic footprint of mutualism: How mutualists influence species' range limits

“…In fact, mutualists often confer benefits in the face of multiple types of stressors. For example, context‐dependent outcomes of fungal endophyte symbiosis in grasses may improve host fitness under drought stress (Afkhami et al, 2014; Donald et al, 2021)—the benefit that expands the distribution of Bromus laevipes by 20%—but also provide protection against biotic stressors such as herbivores (Fuchs & Krauss, 2019), competitors (Vázquez‐de‐Aldana et al, 2013), and pathogens (Pérez et al, 2020). In other systems, different guilds of mutualists may offer benefits to a focal partner along different axes of environmental stress; for example, corals benefit from their symbiotic relationship with photosynthetic algae and can also be defended from herbivores by crustaceans (McKeon et al, 2012).…”

A Systematic Review on the Effects of Epichloë Fungal Endophytes on Drought Tolerance in Cool-Season Grasses

“…No experiment conducted to evaluate the endophyte effect on plant performance under drought uses plant fecundity or seed production as a response variable of fitness. The consideration of the impact of drought on seed production and the transgenerational consequences for progeny performance becomes especially relevant in species associated with vertically transmitted fungal endophytes, since this not only determines the host fitness but also the microorganism persistence (Gundel et al, 2011 , 2017 ; Cavazos et al, 2018 ; Donald et al, 2021 ).…”

“…However, this has yielded contrasting results (Semmartin et al, 2015 ; Gundel et al, 2016 ). A recent paper showed that endophyte infection frequency in a population can be highly dynamic, as variation in the environmental context (accounted for interannual variability in precipitation level) may differentially affect any of the underlying processes that determine the symbiosis prevalence, the differential fitness between endophyte-infected and non-infected plants, and the efficiency with which fungal endophytes are transmitted (Donald et al, 2021 ). Particularly in arid environments, survey studies exploring the occurrence of endophyte-infected plants have constantly shown a low incidence of endophyte-symbiotic plants (Novas et al, 2007 ; Gundel et al, 2011 ; Semmartin et al, 2015 ).…”

“…Particularly in arid environments, survey studies exploring the occurrence of endophyte-infected plants have constantly shown a low incidence of endophyte-symbiotic plants (Novas et al, 2007 ; Gundel et al, 2011 ; Semmartin et al, 2015 ). As the cost–effect relation of the endophyte symbiosis may vary along water availability gradients (Sneck et al, 2017 ; Donald et al, 2021 ), it turns out difficult to establish predictions about the role of endophytes on plant fitness in arid environments based only on the relative performance of plants with and without endophyte under temporary or occasional situations of water shortage. Although plants present specific adaptations to cope with aridity conditions, limitations to primary productivity imposed by permanent situations of water scarcity can make foliar fungal symbionts energetically expensive to maintain (Semmartin et al, 2015 ; Gundel et al, 2016 ).…”

“…Particularly useful would be to combine field survey with manipulative experiments along the species distribution range (e.g., Gibert et al, 2012 ; Afkhami et al, 2014 ) but especially covering the very arid extreme (i.e., ≤ 400 mm year −1 ; Gundel et al, 2016 ). In addition to the challenge of linking physiological mechanisms of plant adaptation (fitness) to the different ecological settings (Volaire, 2018 ), the evaluation of demographic vital rates, such as survival and fecundity, and vertical transmission efficiency of symbionts would allow to identify the endophyte-mediated plant strategies and to better integrate the ecological scales and levels of organization (individual to population; Gundel et al, 2008 ; Donald et al, 2021 ). Besides controlling the endophyte-symbiotic status of plants and water availability, those experiments should also take into account the changes in the genetic structure of symbionts' populations, both of the grass and the fungus species (Keith, 2000 ; Leinonen et al, 2019 ), to unveil the role of fungal endophytes in plant adaptation to extremely arid conditions.…”