Understanding context-dependency in plant–microbe symbiosis: The influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission

Abstract

Understanding the dynamics of a hereditary symbiosis requires testing how ecological factors alter not only the fitness consequences of the symbiosis, but also the rate of symbiont transmission to the next generation. The relative importance of these two mechanisms remains unresolved because studies have not simultaneously examined how the ecological context of the symbiosis influences both costs/benefits and the rate of vertical transmission. Fungal endophytes in grasses have provided particularly tractable systems for investigating the ecological and evolutionary dynamics of hereditary symbiosis. Here we examine interactions between a fungal endophyte, Epichloë amarillans, and its grass host, Agrostis hyemalis, under altered abiotic and biotic contexts: a gradient of water availability and in the presence versus absence of soil microbes. We show that benefits of the symbiosis were strongest when water was limiting. Symbiotic plants at the lowest watering level produced ∼40% more inflorescences and greater seed mass than non-symbiotic plants, while at the highest watering level, symbiotic and non-symbiotic plants did not significantly differ in reproductive fitness. Benefits appear to accrue by allowing hosts to escape from drought, a response that has not been previously reported to be endophyte-mediated. Symbiotic plants at the lowest watering level flowered 9 days earlier than non-symbiotic plants. Interestingly, our results suggest the symbiosis may be costly in the presence of soil microbes, as on live soil, the biomass of symbiotic plants was lower than the biomass of symbiont-free plants. We detected no effect of either the biotic or abiotic context on the rate of symbiont vertical transmission, suggesting that the context-dependent benefits of the symbiosis are the more important driver of variation in symbiont frequency in this system.