Searching for Evidence against the Mutualistic Nature of Hereditary Symbioses: A Comment on Faeth

Rudgers, Jennifer A.; Davitt, Andrew J.; Clay, Keith; Gundel, Pedro E.; Omacini, Marina

doi:10.1086/652996

Cited by 20 publications

(37 citation statements)

References 27 publications

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“…Since Neotyphodium endophytes have lost the capacity for sexual reproduction, their long-term persistence depends entirely on the host's fitness (Clay and Schardl 2002;Saikkonen et al 2004). These hereditary symbioses have generally been regarded as mutualisms (Clay and Schardl 2002;Rudgers et al 2010), although benefits to the host are frequently indirect and are not always clear (Mü ller and Krauss 2005;Cheplick and Faeth 2009). The net outcome for the plant can be understood as the sum of positive and negative endophyte effects, the balance of which is contingent on prevailing conditions (Saikkonen et al 1998;Saona et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Environmental Context of Endophyte Symbioses: Interacting Effects of Water Stress and Insect Herbivory

Miranda

Omacini

Chaneton

2011

International Journal of Plant Sciences

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Symbiotic associations between grasses and fungal endophytes are generally regarded as mutualistic, yet benefits to host plants may vary with environmental context. Previous studies have emphasized how endophytes influence plant responses to single stressors. In contrast, the outcome of endophyte-grass interactions under simultaneous biotic and abiotic stresses remains poorly explored. We hypothesized that benefits from endophyte symbiosis become most apparent in ''complex'' environments where hosts experience multiple stresses. We evaluated the performance of endophyte-infected (Eþ) vs. endophyte-uninfected (EÀ) Lolium multiflorum plants in a factorial experiment with water supply (control vs. drought) and insect herbivory (with aphids vs. without aphids). Endophyte infection delayed tiller production in well-watered plants, while water stress reduced tillering in EÀ plants. Endophyte mediation of herbivory tolerance was contingent on water supply. Whereas aphid herbivory was detrimental to Eþ plants in well-watered soils, aphids interacted with drought stress in decreasing the reproductive output of EÀ but not Eþ plants. Moreover, endophyte presence decreased aphid densities on drought-stressed plants only. Thus, endophyte symbiosis enhanced host tolerance to overlapping biotic and abiotic stresses, although infected plants failed to outgrow their uninfected counterparts. These results support the view that mutualistic endophyte effects may not arise in low-stress environments.

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Section: Introductionmentioning

confidence: 99%

Environmental Context of Endophyte Symbioses: Interacting Effects of Water Stress and Insect Herbivory

Miranda

Omacini

Chaneton

2011

International Journal of Plant Sciences

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“…As their fitness is directly tied to the fitness of their hosts, symbionts can increase in frequency within populations by conferring net benefits to host individuals, such as protection from natural enemies (Sachs et al 2004;Gundel et al 2008;Rudgers et al 2010). In accordance with previous experimental results for other host grass species (reviewed by Clay 1996; Cheplick and Faeth 2009), we found that endophyte presence strongly reduced the density of aphids attacking the native grass Poa autumnalis.…”

Section: Discussionmentioning

confidence: 99%

“…As in other positive species interactions (Bronstein 1994), the benefits conferred by protective symbionts may be conditional on several factors, including the abundance and identity of the host's natural enemies (e.g., Clay et al 2005;Afkhami and Rudgers 2009) as well as resource availability and the abiotic environment (reviewed by Cheplick and Faeth 2009). Protection interactions are perhaps more likely to be context-dependent than symbioses providing direct (e.g., nutritional) rewards because the presence/ abundance of a third species (the host enemy) is required for benefits to accrue, thus forming an indirect species interaction (Bronstein 1998;Rudgers et al 2010). However, relatively few studies have investigated factors affecting the strength of benefits conferred by most types of protection symbioses, with the exception of ant-plant interactions (reviewed by Bronstein 1998).…”

Section: Introductionmentioning

confidence: 99%

Water availability alters the tri-trophic consequences of a plant-fungal symbiosis

Yule

Woolley

Rudgers

2010

Arthropod-Plant Interactions

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Plant-microbe protection symbioses occur when a symbiont defends its host against enemies (e.g., insect herbivores); these interactions can have important influences on arthropod abundance and composition. Understanding factors that generate context-dependency in protection symbioses will improve predictions on when and where symbionts are most likely to affect the ecology and evolution of host species and their associated communities. Of particular relevance are changes in abiotic contexts that are projected to accompany global warming. For example, increased drought stress can enhance the benefits of fungal symbiosis in plants, which may have multi-trophic consequences for plant-associated arthropods. Here, we tracked colonization of fungal endophyte-symbiotic and aposymbiotic Poa autumnalis (autumn bluegrass) by Rhopalosiphum padi (bird-cherry-oat aphids) and their parasitoids (Aphelinus sp.) following manipulations of soil water levels. Endophyte symbiosis significantly reduced plant colonization by aphids. Under low water, symbiotic plants also supported a significantly higher proportion of aphids that were parasitized by Aphelinus and had higher aboveground biomass than aposymbiotic plants, but these endophyte-mediated effects disappeared under high water. Thus, the multi-trophic consequences of plant-endophyte symbiosis were contingent on the abiotic context, suggesting the potential for complex responses in the arthropod community under future climate shifts.

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“…Endophytes of native grasses can negatively affect host performance by reducing competitive ability (Faeth et al 2004), growth and reproduction (Faeth and Sullivan 2003). Specifically, they can alter host resource allocation to increase their own transmission, which sometimes reduces allocation to plant reproduction (Faeth 2009;Gorischek et al 2013;but see Faeth 2010;Rudgers et al 2010). Conversely, the positive effects of endophytes range from increased competitive ability (Vázquez-de-Aldana et al 2012) and allelopathy (Vázquez-de-Aldana et al 2011) to decreased preference and performance of herbivores on infected grasses (Crawford et al 2010).…”

Section: Introductionmentioning

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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Searching for Evidence against the Mutualistic Nature of Hereditary Symbioses: A Comment on Faeth

Cited by 20 publications

References 27 publications

Environmental Context of Endophyte Symbioses: Interacting Effects of Water Stress and Insect Herbivory

Environmental Context of Endophyte Symbioses: Interacting Effects of Water Stress and Insect Herbivory

Water availability alters the tri-trophic consequences of a plant-fungal symbiosis

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

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