Neotyphodiumendophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency

Abstract

Persistence and ubiquity of vertically transmitted Neotyphodium endophytes in grass populations is puzzling because infected plants do not consistently exhibit increased fitness. Using an annual grass population model, we show that the problems for matching endophyte infection and mutualism are likely to arise from difficulties in detecting small mutualistic effects, variability in endophyte transmission efficiency and an apparent prevalence of non-equilibrium in the dynamics of infection. Although endophytes would ultimately persist only if the infection confers some fitness increase to the host plants, such an increase can be very small, as long as the transmission efficiency is sufficiently high. In addition, imperfect transmission limits effectively the equilibrium infection level if the infected plants exhibit small or large reproductive advantage. Under frequent natural conditions, the equilibrium infection level is very sensitive to small changes in transmission efficiency and host reproductive advantage, while convergence to such an equilibrium is slow. As a consequence, seed immigration and environmental fluctuation are likely to keep local infection levels away from equilibrium. Transient dynamics analysis suggests that, when driven by environmental fluctuation, infection frequency increases would often be larger than decreases. By contrast, when due to immigration, overrepresentation of infected individuals tends to vanish faster than equivalent overrepresentation of noninfected individuals.

Heritable symbionts in a world of varying temperature

“…Variation in vertical transmission efficiency is thought to be an important driver of endophyte dynamics and equilibrium prevalence, as the 'benefit' from endophyte infection is relatively weak (Afkhami and Rudgers, 2008;Gundel et al, 2008). However, although loss in seed storage argues for a role of temperature in endophyte dynamics, exploration of the whole transmission cycle under natural conditions is required to determine the sensitivity of endophyte dynamics to thermal environment: loss of endophyte infection can occur at any of three stages-from tiller to seed, seed to seedling and during tiller growth (Afkhami and Rudgers, 2008).…”

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

“…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).…”

“…Counterintuitively, strong host-symbiont mutualism may actually facilitate persistence of symbiont-free hosts if it is also associated with niche differentiation. Imperfect transmission (Gundel et al 2008) and migration (Saikkonen et al 2002) could further cloud connections between fitness effects of symbionts and local symbiont frequency, as others have recognized (Cheplick and Faeth 2009), and modeling their influence can provide additional insights. Thus, observed symbiont frequencies are, at best, incomplete information about the fitness effects of symbionts on hosts and, at worst, completely mute on the issue.…”

“…Explanations for variable and intermediate symbiont frequencies have primarily invoked mechanisms based on linear (density-independent) population dynamics, notably imperfect transmission (Gundel et al 2008) but also including migration (Saikkonen et al 2002) and nonequilibrium dynamics (Clay 1993 mission. Density-dependent competition was stronger within versus between symbiotic and symbiont-free hosts, indicative of niche differentiation.…”

“…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.…”