A fungus among us: broad patterns of endophyte distribution in the grasses

Abstract

Plant-associated microbes have been increasingly recognized for influencing host populations, plant communities, and even herbivores and predators. Thus, understanding factors that affect the distribution and abundance of microbial symbioses may be important for predicting the ecological dynamics of communities. Using endophytic fungi-grass symbioses, we explored how intrinsic traits of the symbiosis, specifically transmission mode, may influence symbiont frequencies in host populations. Combining published literature with new field surveys, we compared Epichloë endophytes, which had mixed horizontal and vertical transmission, with Neotyphodium endophytes, which were exclusively vertically transmitted from host plants to seeds. Exclusively vertical transmission should select against pathogenicity because symbionts depend entirely on hosts for reproduction. Across 118 host species, we found that Neotyphodium hosts had 40-130% higher symbiont frequencies than Epichloë hosts. In field surveys, endophyte frequency was positively correlated with the local density of hosts, but only for Epichloë, suggesting that contagiously spread Epichloë may attain higher frequencies when hosts are more abundant. Epichloë endophytes were also more likely than Neotyphodium to have imperfect vertical transmission; thus, hosts may reduce the transmission of more pathogenic symbionts to seeds. Results are consistent with the conclusion that the evolutionary transition to exclusively vertical transmission can alter patterns of symbiont frequency in nature.

Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions

“…Aspects of specialization from genetic architecture to interaction complexity could all fall under the influence of viruses, bacteria, and fungi residing in hosts (Rudgers et al 2009, Gibson and Hunter 2010, Vogel and Moran 2011.…”

Inherited fungal symbionts enhance establishment of an invasive annual grass across successional habitats

“…About 30% of pooid grass species are maternally infected with systemic fungal endophytes (Clay and Schardl 2002;Cheplick and Faeth 2009), and hence carry their microbial symbionts upon dispersal from the parent plant. Although several invasive grasses are known to be associated with fungal endophytes (see Rudgers et al 2009), these cryptic leaf symbionts have been largely overlooked in the context of invasions (Desprez-Loustau et al 2007;van der Putten et al 2007), and only recently have been regarded as potential mediators of invasion dynamics (Rudgers et al , 2007. Most work to date focussed on the impact of endophyte-grass associations on resident communities after the host population already became widely established (Clay et al 2005;Omacini et al 2005;Rudgers et al 2007).…”

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

“…Due to this fitness feedback mechanism, symbionts that have positive effects on their hosts are expected to become fixed in host populations, and parasitic symbionts are expected to be eliminated (e.g., Clay 1993). Despite these expectations, evidence for intermediate symbiont frequency is widespread (Tsuchida et al 2002;Davidson and Stahl 2006;Rudgers et al 2009;Iannone et al 2011). For example, the population-level frequency of the vertically transmitted bacterium Wolbachia follows a bimodal distribution across species of arthropod host, with peaks at 0% and 100% but a broad range of infection levels between these extremes (Hilgenboecker et al 2008).…”

“…For example, the population-level frequency of the vertically transmitted bacterium Wolbachia follows a bimodal distribution across species of arthropod host, with peaks at 0% and 100% but a broad range of infection levels between these extremes (Hilgenboecker et al 2008). Similarly, for the vertically transmitted fungal endophytes of many grasses, intermediate symbiont frequencies seem to be more the rule than the exception (reviewed in Cheplick and Faeth 2009;Rudgers et al 2009). Variable and often intermediate symbiont frequencies have contributed to confusion over whether vertically transmitted symbionts function primarily as mutualists, as predicted by evolutionary theory, or as parasites (Faeth 2002;Faeth et al 2004).…”

“…Epichloid endophytes produce alkaloids that can confer host resistance to various stresses, including herbivory (Schardl et al 2004). Despite potential for benefits of endophyte symbiosis, evidence from natural populations indicates that intermediate endophyte frequencies are widespread (Rudgers et al 2009). In A. hyemalis, for example, populationlevel endophyte frequency ranges from 0% to 100% with a mean of 69% symbiotic individuals (Rudgers et al 2009).…”