Genetically based vertical transmission drives the frequency of the symbiosis between grasses and systemic fungal endophytes

Gibert, Anaïs; Hazard, Laurent

doi:10.1111/1365-2745.12073

Cited by 18 publications

(17 citation statements)

References 51 publications

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“…Conversely, the systemic Clavicipitaceous leaf fungal endophytes of grasses have been significantly less considered (Omacini et al 2012). These endophytes profoundly affect grass population dynamics and adaptation to changing ecological environments, with ultimate consequences on plant communities and ecosystems processes (Saikkonen et al 1998;Omacini et al 2001Omacini et al , 2012Clay & Schardl 2002;Rudgers, Koslow & Clay 2004;Gibert & Hazard 2013).…”

Section: Introductionmentioning

confidence: 99%

Broad‐scale variation of fungal‐endophyte incidence in temperate grasses

et al. 2015

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Summary1. The strength of many interactions between plants and other organisms changes across regional gradients. For example, the relevance of plant-herbivore interactions increases with primary production. Likewise, biotic interactions collectively become more intense from the poles to the equator. Yet, the regional variation of the interaction between grasses and systemic fungal endophytes, which provide resistance to biotic and abiotic environmental factors (i.e. herbivory and drought), is poorly understood. 2. We compiled 1008 records of the incidence level of fungal endophytes (Epichlo€ e, Ascomycetes: Clavicipitaceae) on wild populations of 48 cool season grasses, encompassing 10 biomes across a broad latitudinal expanse and primary production gradient. Symbiosis incidence was analysed as a function of mean primary production, precipitation, temperature and latitude of each site, which in turn were obtained from climatic and satellital sources. 3. Across a 30-fold variation of mean primary production, average symbiosis incidence increased from 20% to 70%. The pattern became stronger when the analysis was restricted to the single grass genus Festuca, which accounted for half of the total data. 4. The number of grass populations showing no symbiosis incidence (0%) decreased as primary production increased, whereas those with 100% of incidence increased. 5. Primary production at the regional scale was negatively correlated with latitude but positively with mean annual temperature and precipitation. Symbiosis incidence was similarly correlated with latitude and temperature, and it was not with mean annual precipitation. 6. Synthesis. Different descriptors of this grass-fungus symbiosis show that average incidence in wild populations world-wide increases with mean primary production. As at large spatial scales herbivory and temperature increase and aridity decreases with primary production, our results suggest that, at broad-scales, these biotic and abiotic factors may be important drivers of the symbiosis success.

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Section: Introductionmentioning

confidence: 99%

Broad‐scale variation of fungal‐endophyte incidence in temperate grasses

et al. 2015

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“…For example in a recent study, the presence of grazing reduced the proportion of infected seeds produced by infected Lolium multiflorum (García-Parisi et al 2012). Furthermore, the proportion of endophyte-infected seeds produced by infected parental plants is often positively correlated with endophyte frequencies within populations (Afkhami and Rudgers 2008;Gibert and Hazard 2013). In our system, a combination of reduced seed production and endophyte transmission fidelity may maintain lower infection frequencies in younger, more recently grazed exclosures.…”

Section: Alternate Hypotheses Explaining Endophyte Dynamics In the Fieldmentioning

confidence: 95%

“…Imperfect vertical transmission of endophytes often depends most strongly on plant genetic background (Davitt et al 2011;Gundel et al 2011a;Gibert and Hazard 2013), although there is some evidence that biotic interactions (e.g., grazing) can influence endophyte transmission fidelity. For example in a recent study, the presence of grazing reduced the proportion of infected seeds produced by infected Lolium multiflorum (García-Parisi et al 2012).…”

Section: Alternate Hypotheses Explaining Endophyte Dynamics In the Fieldmentioning

confidence: 99%

Fungal endophytes of Festuca rubra increase in frequency following long-term exclusion of rabbits

Santangelo

Turley

Johnson

2015

Botany

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Plant -fungal endophyte interactions are common in nature and they can shape the ecology of plants. Vertically transmitted endophytes are hypothesized to serve as mutualists, protecting plants from herbivores. If this hypothesis is true, then we expect endophytes to be most abundant in the presence of herbivores and least abundant in their absence, assuming endophytes incur a cost to their host. We tested this prediction by studying the effects of intense rabbit (Oryctolagus cuniculus Linnaeus) grazing on grass-endophyte interactions at Silwood Park, UK. We examined seeds of red fescue (Festuca rubra L.) collected from 15 natural populations that were protected from rabbits for 0.3-21 years. Contrary to our prediction, the mean proportion of seeds with endophytes increased 1.84×, from 0.45 to 0.83, following 21 years of rabbit exclusion. To better understand the mechanisms driving this increase in frequency, we conducted a fully factorial greenhouse experiment where we manipulated the presence or absence of endophyte infection, intraspecific competition, and simulated grazing on F. rubra plants.In both damaged and undamaged treatments, infected plants produced approximately twice as much biomass as uninfected plants, and endophytes did not influence tolerance to herbivory. These results suggest that endophytes directly change plant growth but not compensatory responses to damage. In the absence of competitors, infected plants produced 2.17× more biomass than uninfected plants, whereas in the presence of competitors, infected plants produced only 1.55× more biomass than uninfected plants. This difference suggests that intraspecific competition might lessen the benefits of endophyte infection. Our results do not support the defensive mutualism hypothesis, but instead suggest that endophyte-induced plant growth is important in shaping the costs and benefits of endophytes in our system. Résumé :Les interactions plante -endophyte fongique sont fréquentes dans la nature et elles peuvent façonner l'écologie des végétaux. Les endophytes transmis de manière verticale sont présumés servir d'organismes mutualistes, protégeant les végétaux des herbivores. Si cette hypothèse s'avère, on peut conséquemment s'attendre à ce que les endophytes soient plus abondants en présence d'herbivores et moins abondants en leur absence, assumant que les endophytes engagent un coût pour leur hôte. Les auteurs ont testé cette prédiction en étudiant les effets d'un broutage intense par le lapin (Oryctolagus cuniculus Linnaeus) sur les interactions herbes-endophytes à Silkwood Park, RU. Ils ont examiné les graines de la fétuque rouge (Festuca rubra L.) recueillies de 15 populations naturelles protégées des lapins pendant 0,3-21 ans. Contrairement à leur prédiction, la proportion moyenne de graines comprenant des endophytes augmentait de 1,84×, de 0,45 à 0,83, après avoir exclu les lapins pendant 21 ans. Afin de mieux comprendre les mécanismes responsables de cette augmentation de la fréquence, les auteurs ont réalisé des expériences factorielles...

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“…Theoretical models show that imperfect transmission can stabilize intermediate infection frequencies, even when symbionts confer a strong fitness advantage, because there is a persistent source of nonsymbiotic hosts each generation (Turelli 1994;Ravel et al 1997;Gundel et al 2008). Empirical studies have confirmed that imperfect symbiont transmission is widespread in plant and animal hosts (e.g., Hurst et al 2001;Moran and Dunbar 2006;Afkhami and Rudgers 2008;Gundel et al 2011) and contributes to intermediate symbiont frequencies in natural populations (Gibert and Hazard 2013;Yule et al 2013). Like most symbiosis theory, the imperfect transmission hypothesis assumes linear population dynamics, whereby fitness and transmission parameters are unaffected by population density.…”

Section: Introductionmentioning

confidence: 99%