- Genotype-specific interactions and the trade-off between host and parasite fitness

Understanding the selective forces driving parasite evolution is crucial in the fight against infectious diseases, both in agriculture and human health. Darwinian medicine aims at controlling the evolution of human pathogens in order to drive them toward "milder" forms or, ideally, to extinction [1]. Such control requires knowledge of which traits of infections are adaptive for the host or the parasite as well as the associated trade-offs between traits and constraints on their evolution. Indeed, parasites harm their hosts in a number of ways that may be adaptive or not [2]. One source of negative effects of parasites on their hosts, adaptive to the parasites themselves, is the consumption of host resources by parasite growth and reproduction. Because host resources that are diverted by parasites are no longer available to the host, this must lead to a reduction in host fitness, termed virulence. If parasites that reproduce or transmit more do so by appropriating more host resources they should have stronger negative effects on their host, leading to a positive relationship between a parasite's transmission and its virulence, as is both predicted [2-5] and observed [[6], but see [7]]. From the point of view of the host, this would be expressed as a negative relationship between parasite transmission and host fitness [8,9]. Examining this relationship, i.e. how host fitness varies with parasite transmission success, has certain advantages because the different measures of virulence among studies are not always easily comparable nor do they necessarily imply the same thing for host or parasite fitness (e.g., host mortality versus weight loss).

When increased parasite virulence results in increased parasite transmission, modifying transmission may influence the evolutionary trajectory of virulence. This forms the theoretical basis for virulence management that proposes to modify virulence by altering transmission [10,11], though its practical applicability for disease management in natural systems is still hotly debated [6,12,13]. Indeed, some selection experiments have failed to observe an evolution of virulence in the predicted direction [14,15] even when using a single host genotype, thereby avoiding the complications due to the specificity of the infection phenotype among specific host and parasite combinations [16]. To date, environmental and/or host genetic variation are rarely taken into account when quantitative parasite traits are investigated though virulence and transmission ability are not traits of the parasite in isolation, depending on the host and environment it encounters [17-20], as has been commonly accepted for infection ability in plant-pathogen systems [21,22] or other host-parasite associations [23-25]. Therefore, to understand how parasite transmission affects host fitness we need to examine this relationship across a range of parasite and host genotypic combinations to better assess the role of each player in the host-parasite game and the nature of their shared phenotypic traits.

Here we examine the relationship between parasite and host fitness using all compatible combinations between seven parasite strains of the specialist oomycete, Hyaloperonospora arabidopsis (= parasitica) and six lines of its natural host Arabidopsis thaliana (Brassicaceae). With this experimental procedure we avoid as much as possible the variation due to gene-for-gene interactions for the qualitative compatibility between host and parasite genotypes, in order to concentrate on variation for quantitative phenotypic traits. H. arabidopsis is not lethal for its host, which enables us to measure both host and parasite fitness as the production of propagules, respectively seeds and asexual conidiospores. Furthermore, the fitness of an uninfected host gives a benchmark measure for how a healthy host would expend available resources on seed production and we test whether parasites that have increasing success in transmission are diverting increasing amounts of resources away from this primary goal for the host, both as a general tendency and in a specific way for different host or parasite genotypes.

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