Local adaptation at higher trophic levels: contrasting hyperparasite-pathogen infection dynamics in the field and laboratory

Abstract

Predicting and controlling infectious disease epidemics is a major challenge facing the management of agriculture, human and wildlife health. Co-evolutionarily derived patterns of local adaptation among pathogen populations have the potential to generate variation in disease epidemiology; however, studies of local adaptation in disease systems have mostly focused on interactions between competing pathogens or pathogens and their hosts. In nature, parasites and pathogens are also subject to attack by hyperparasitic natural enemies that can severely impact upon their infection dynamics. However, few studies have investigated whether this interaction varies across combinations of pathogen-hyperparasite strains, and whether this influences hyperparasite incidence in natural pathogen populations. Here, we test whether the association between a hyperparasitic fungus, Ampelomyces, and a single powdery mildew host, Podosphaera plantaginis, varies among genotype combinations, and whether this drives hyperparasite incidence in nature. Laboratory inoculation studies reveal that genotype, genotype × genotype interactions and local adaptation affect hyperparasite infection. However, observations of a natural pathogen metapopulation reveal that spatial rather than genetic factors predict the risk of hyperparasite presence. Our results highlight how sensitive the outcome of biocontrol using hyperparasites is to selection of hyperparasite strains.

Keywords: co-evolution; disease; host-parasite interactions; hyperparasite; local adaptation.

Figure 1

Ampelomyces is common at the metapopulation level. Map of the 70 Po. plantaginis populations in Åland that were screened during 2014. Of these, 54 were found to be infected by the Ampelomyces hyperparasite (pink circles). The 15 sites indicated with blue triangles were intensively surveyed across the whole summer of 2014.

Figure 2

Hyperparasite infectivity and infection severity varied among pathogen–hyperparasite genotype combinations. Hyperparasite strain 294_11 performed better than both other strains in terms of both the proportion of mildew lesions it infected, and the extent of infection after 16 days of growth. Mildew strains also vary in their susceptibility to hyperparasite attack, which is dependent upon the identity of the hyperparasite. For instance, mildew 33B is highly susceptible to 294_11 and 9066_3, but is able to resist 3210_3_2.

Figure 3

Ampelomyces can be locally adapted to its mildew host. Hyperparasite infectivity and infection severity strongly varied among hyperparasite strains (individual plots) and between sympatric/allopatric mildew hosts. Statistical analysis suggests that Ampelomyces was more infective against sympatric mildew than the mean of all allopatric combinations; however, the presence and intensity of this effect varied greatly among hyperparasite genotypes. This could indicate that selection for local adaptation varies in strength across the metapopulation, or that the strength of selection is highly dynamic over evolutionary time.

Figure 4

Ampelomyces infections are spatially clustered among mildew‐infected plants within populations. Facets represent geometric area of the 14 intensively surveyed Po. plantaginis populations in which at least one mildew‐infected leaf supported a hyperparasite infection. Circles denote the locations of mildew‐infected Plantago lanceolata. Pink circles denote host plants from which at least one mildew sample was found to support the hyperparasite.

Figure 5

Factors influencing within‐population Ampelomyces prevalence. Ampelomyces infections are significantly positively correlated with the connectivity of Ampelomyces‐infected plants (A) and also significantly more common on leaves supporting >1 mildew MLG (B). There is a positive, but not significant correlation between the amount of mildew surrounding a focal plant and its probability of supporting Ampelomyces (C). Mildew MLG identity does not significantly predict Ampelomyces presence, although hyperparasite infectivity does vary across MLGs (D).