Abstract

Two main mechanisms are thought to affect the prevalence of endophyte-grass symbiosis in host populations: the mode of endophyte transmission, and the fitness differential between symbiotic and non-symbiotic plants. These mechanisms have mostly been studied in synthetic grass populations. If we are to improve our understanding of the ecological and evolutionary dynamics of such symbioses, we now need to determine the combinations of mechanisms actually operating in the wild, in populations shaped by evolutionary history. We used a demographic population modeling approach to identify the mechanisms operating in a natural stand of an intermediate population (i.e. 50% of plants symbiotic) of the native grass Festuca eskia. We recorded demographic data in the wild over a period of three years, with manipulation of the soil resources for half the population. We developed two stage-structured matrix population models. The first model concerned either symbiotic or non-symbiotic plants. The second model included both symbiotic and non-symbiotic plants and took endophyte transmission rates into account. According to our models, symbiotic had a significantly higher population growth rate than non-symbiotic plants, and endophyte prevalence was about 58%. Endophyte transmission rates were about 0.67 or 0.87, depending on the growth stage considered. In the presence of nutrient supplementation, population growth rates were still significantly higher for symbiotic than for non-symbiotic plants, but endophyte prevalence fell to 0%. At vertical transmission rates below 0.10–0.20, no symbiosis was observed. Our models showed that a positive benefit of the endophyte and vertical transmission rates of about 0.6 could lead to the coexistence of symbiotic and non-symbiotic F. eskia plants. The positive effect of the symbiont on host is not systematically associated with high transmission rates of the symbiont over short time scales, in particular following an environmental change.

Highlights

  • Symbioses have been implicated in many of the major ecological and evolutionary innovations in the history of life [1]

  • Our findings suggest that symbiotic and non-symbiotic plants can coexist in a stable manner within grass populations, due to the combination of a positive effect of the endophyte on host fitness, and imperfect vertical transmission

  • We demonstrated that changes to nutrient resources dissociated the transmission rate of the endophyte from its effects, leading to the disappearance of the endophyte from the host population

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Summary

Introduction

Symbioses have been implicated in many of the major ecological and evolutionary innovations in the history of life [1]. Mitochondria and chloroplasts have become fixed across host populations and generations, whereas this is not the case for contemporary symbioses such as the fungus Neotyphodium in grasses (for a review [4]) or the bacterium Wolbachia in arthropods [5]. Consider the fungus from the genera Neotyphodium and Epichloë (Clavicipitaceae, Ascomycota) as an illustration These vertically transmitted fungal endophytes are prevalent in cool-season grasses. These vertically-transmitted fungal endophytes commonly display a mosaic of prevalence, ranging from 0 to 100%, in host populations [8,9,10,11] Does this imply that contemporary symbioses are not sufficiently beneficial to their hosts to have become fixed? Investigations of the interplay between symbiont transmission and effects in the generation of current prevalence patterns are required to improve our understanding of why some symbioses are fixed in host species, whereas others are not

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