Testing the roles of vertical transmission and drought stress in the prevalence of heritable fungal endophytes in annual grass populations

Abstract

Beneficial inherited symbionts are expected to reach high prevalence in host populations, yet many are observed at intermediate prevalence. Theory predicts that a balance of fitness benefits and efficiency of vertical transmission may interact to stabilize intermediate prevalence. We established populations of grass hosts (Lolium multiflorum) that varied in prevalence of a heritable fungal endophyte (Epichloё occultans), allowing us to infer long-term equilibria by tracking change in prevalence over one generation. We manipulated an environmental stressor (elevated precipitation), which we hypothesized would reduce the fitness benefits of symbiosis, and altered the efficiency of vertical transmission by replacing endophyte-positive seeds with endophyte-free seeds. Endophytes and elevated precipitation both increased host fitness, but symbiont effects were not stronger in the drier treatment, suggesting that benefits of symbiosis were unrelated to drought tolerance. Reduced transmission suppressed the inferred equilibrium prevalence from 42.6% to 11.7%. However, elevated precipitation did not modify prevalence, consistent with the result that it did not modify fitness benefits. Our results demonstrate that failed transmission can influence the prevalence of heritable microbes and that intermediate prevalence can be a stable equilibrium due to forces that allow symbionts to increase (fitness benefits) but prevent them from reaching fixation (failed transmission).

Ontogenetic and trans‐generational dynamics of a vertically transmitted fungal symbiont in an annual host plant in ozone‐polluted settings

“…The results from this study are relevant for understanding the ecological dynamics of the plant-endophyte symbiosis in natural and managed ecosystems. Vertical transmission efficiency, which also involves endophyte persistence in seed, is an important process controlling the incidence of Epichloë fungal endophytes in grass populations (Afkhami & Rudgers, 2008;Cavazos et al, 2018;Gundel, Garibaldi, et al, 2011;Gundel, Rudgers, et al, 2011). In addition, this study showed that there was an alignment of the partners' fitness; the higher the seed production, the higher multiplication rate of the fungus and higher concentration of alkaloids in seed.…”

Maternal effects and environmental filtering shape seed fungal communities in oak trees

“…Future research will have to investigate the maternal and environmental drivers of the rate of vertical transmission of microorganisms (e.g. Cavazos et al , 2018; Sneck et al , 2017; Leff et al , 2017), and assess the role of these microorganisms on seed survival and germination, seedling growth and health (e.g. Vivas et al , 2017; Leroy et al , 2019), and ultimately tree fitness.…”

Testing for loss of Epichloë and non‐epichloid symbionts under altered rainfall regimes

“…Symbionts can allow their hosts to cope with global change (Kivlin et al, 2013;Cavazos et al, 2018), yet our work suggests that associations with the Epichloë endophyte can be gradually lost over time with reduced precipitation. These findings could suggest that A. breviligulata's association with Epichloë may be particularly costly under drought conditions or that Epichloë itself may be unable to persist in drought-exposed host plants.…”

“…non-epichloid taxa to colonize (Zimmerman and Vitousek, 2012;Giauque and Hawkes, 2013), but will not directly affect the arrival and establishment of vertically transmitted Epichloë (Rodriguez et al, 2009). Maintaining symbiosis with Epichloë will typically depend on the costs and benefits of symbiosis in the novel environmental context and the rate of vertical transmission (Cheplick, 2007;Davitt et al, 2010;Emery et al, 2010;Gundel et al, 2011;Yule et al, 2013;Cavazos et al, 2018).…”