Costs, Benefits, Parasites and Mutualists: The Use and Abuse of the Mutualism-Parasitism Continuum Concept for Epichloë Fungi

Abstract

The species comprising the fungal endophyte genus Epichloe are symbionts of cool season grasses. About half the species in this genus are strictly vertically transmitted, and evolutionary theory suggests that these species must be mutualists. Nevertheless, Faeth and Sullivan (e.g. 2003) have argued that such vertically transmitted endophytes are "usually parasitic," and Muller and Krauss (2005) have argued that such vertically transmitted endophytes fall along a mutualism-parasitism continuum. These papers (and others) have caused confusion in the field. We used a systematic review to show that close to half of the published papers in this field incorrectly categorize the interaction. Here, we develop the argument that advantages and disadvantages are not the same things as mutualism and parasitism and that experimental evidence must be interpreted in the context of theory. We argue that, contra Faeth and Sullivan, it is highly unlikely that such strictly vertically transmitted endophytes can be parasites, and that, contra Muller and Krauss, it is inappropriate to apply the continuum concept to strictly vertically transmitted endophytes. We develop a mathematical model to support and illustrate our arguments. We use the model to clarify that parasitism requires some degree of horizontal transmission, and that while it is appropriate to use the continuum concept when referring to the genus as a whole, or to species that possess horizontal transmission, we argue that it is inappropriate to use the concept when referring to species that are strictly vertically transmitted.