Genotype-specific benefits and risks of a mutualist association during natural epidemics

Abstract

While both plant-associated pathogenic and mutualistic microbes are ubiquitous across ecosystems, how they interact to determine disease risk in natural, genetically diverse populations is not known. To test whether mycorrhizal fungi provide protection against infection, and whether this functions in a genotype-specific manner, we conducted a field experiment in three naturally-occurring epidemics of a fungal pathogen, Podosphaera plantaginis, infecting a host plant, Plantago lanceolata, in the Åland Islands, Finland. In each population, we collected field epidemiological data on mycorrhizal-inoculated and non-mycorrhizal experimental plants originating from six allopatric populations. Mycorrhizal association caused host genotype-specific changes in growth and infection rates in the host populations, but reduced infection severity in hosts from every genetic origin. Protection occurred via changes in the relationship between growth and infection in the host individuals: mycorrhizal individuals grew larger without increasing their infection risk or load. More susceptible host genotypes received stronger protective effects from mycorrhizae. Our results show that mycorrhizal fungi produce host genotype-specific growth and defensive benefits and alter infection risks in wild host populations. Understanding how mutualism-derived protection alters host susceptibility to disease will be important for predicting infection outcomes in ecological communities and in agriculture.