There are many ways to be a mutualist: Endophytic fungus reduces plant survival but increases population growth

Abstract

One of the challenges to quantifying the costs and benefits of symbiosis is that symbionts can influence different components of host fitness. To improve understanding of the ecology of inherited symbionts, we developed general theory for a perennial host-hereditary symbiont interaction, in which symbionts can have independent and potentially opposing effects on host regeneration and survival. The model showed that negative effects on one component of fitness may be outweighed by positive effects on another, leading to a net positive impact of symbiosis on population growth. Model predictions depended on the availability of suitable patches, which influenced the relative contributions of survival vs. regeneration to host fitness. We then used experimental symbiont removal to quantify effects of a hereditary, fungal endophyte on a grass host. Endophyte presence strongly reduced host survival but increased regeneration. Application of the model revealed that negative effects on plant survival were overwhelmed by beneficial effects on regeneration, resulting in stable endophyte persistence at 100% frequency, consistent with field observations. Our work demonstrates the utility of a demographic perspective for predicting the dynamics of symbioses and supports the hypothesis that symbionts function as mutualists when host and symbiont fitness are coupled through vertical transmission.

Balancing anti‐herbivore benefits and anti‐pollinator costs of defensive mutualists

“…There is growing evidence that longevity and life cycle complexity can buffer iteroparous organisms against costs of mutualism. For example, negative effects of fungal symbionts on the survival of perennial grasses can be more than offset by positive effects of symbionts on growth (Yule et al 2013) or reproduction (Rudgers et al 2012), resulting in stable mutualism. Similarly, Palmer et al (2010) showed that long-lived Acacia trees can sustain negative effects of ant symbionts on low-elasticity vital rates and still gain net fitness benefits if those costs are balanced by positive effects on high-elasticity rates.…”

“…Long-lived plants may tolerate reproductive costs of ant defense without a reduction in fitness if they also experience benefits in terms of growth and survival (Stanton and Palmer 2011). Demographic models are essential for assessing the balance of costs and benefits in the currency of fitness, but their implementation for this purpose is surprisingly rare (Palmer et al 2010, Rudgers et al 2012, Yule et al 2013. Furthermore, because the occurrence of ant defense and the identity of ant partners may change over the lifetime of an individual plant (Young et al 1997, Fonseca and Benson 2003, Palmer et al 2010, Miller and Rudolf 2011, assessing the fitness effects of each species in isolation may be too simplistic.…”

Niche Differentiation in the Dynamics of Host-Symbiont Interactions: Symbiont Prevalence as a Coexistence Problem

“…Vertically transmitted symbioses are widespread across the tree of life, including the heritable microbes common in terrestrial arthropods (Engelstädter and Hurst 2009) and marine invertebrates (e.g., Sharp et al 2007) as well as the rich microbiomes of vertebrates (Ley et al 2008). Heritable symbionts can affect the fitness and population dynamics of their hosts (Rudgers et al 2012;Yule et al 2013) and the communities and ecosystems in which they reside (Clay and Holah 1999;Knowlton and Rohwer 2003). They are also responsible for some of the most important evolutionary innovations in the history of life, such as the chloroplasts of plants and mitochondria of eukaryotes (Margulis 1996).…”

“…Thus far, predictions for how competition should influence symbiont frequency have focused on the mean fitness effects of symbionts (Clay 1993;Gundel et al 2008;Rudgers et al 2012), including the dependence of fitness effects on environmental variables such as herbivore pressure (Clay et al 2005). However, symbionts can have important effects on the physiology and ecology of their hosts and available evidence suggests that they can modify niche characteristics.…”

“…Epichloid fungal endophytes, primarily in the genera Neotyphodium and Epichloë, are estimated to occur in up to 30% of grass species (Leuchtmann 1992). In cases where grass and endophyte fitnesses are tightly coupled via exclusively vertical transmission, these symbionts are thought to function primarily as mutualists (e.g., Rudgers et al 2012), although interaction outcomes may depend upon environmental context (Davitt et al 2011;Miranda et al 2011). Epichloid endophytes produce alkaloids that can confer host resistance to various stresses, including herbivory (Schardl et al 2004).…”