A hyperparasite affects the population dynamics of a wild plant pathogen

Abstract

Assessing the impact of natural enemies of plant and animal pathogens on their host's population dynamics is needed to determine the role of hyperparasites in affecting disease dynamics, and their potential for use in efficient control strategies of pathogens. Here, we focus on the long-term study describing metapopulation dynamics of an obligate pathogen, the powdery mildew (Podosphaera plantaginis) naturally infecting its wild host plant (Plantago lanceolata) in the fragmented landscape of the Åland archipelago (southwest Finland). Regionally, the pathogen persists through a balance of extinctions and colonizations, yet factors affecting extinction rates remain poorly understood. Mycoparasites of the genus Ampelomyces appear as good candidates for testing the role of a hyperparasite, i.e. a parasite of other parasites, in the regulation of their fungal hosts' population dynamics. For this purpose, we first designed a quantitative PCR assay for detection of Ampelomyces spp. in field-collected samples. This newly developed molecular test was then applied to a large-scale sampling within the Åland archipelago, revealing that Ampelomyces is a widespread hyperparasite in this system, with high variability in prevalence among populations. We found that the hyperparasite was more common on leaves where multiple powdery mildew strains coexist, a pattern that may be attributed to differential exposure. Moreover, the prevalence of Ampelomyces at the plant level negatively affected the overwinter survival of its fungal host. We conclude that this hyperparasite may likely impact on its host population dynamics and argue for increased focus on the role of hyperparasites in disease dynamics.

Pathogen dynamics under both bottom‐up host resistance and top‐down hyperparasite attack

“…Here, hyperparasitism significantly reduced the production of overwintering structures. This may explain why previous studies have found a link between hyperparasitism and powdery mildew extinction risk in nature (Tollenaere et al., ). Combined, our results suggest that top‐down control of pathogens by natural enemies may be sensitive to both the combination of pathogen and host genotype, and the specific pathogen life‐history stage that is targeted.…”

“…Field surveys have shown that Ampelomyces infections are detectable early during mildew epidemics (Parratt et al., and Supporting Information Figure ), and severely reduce overwinter survival of Po. plantaginis in nature (Tollenaere et al., ). In other mildew species, Ampelomyces reduces conidial production and reverses mildew‐derived tissue damage in hosts under controlled conditions (Abo‐Foul, Raskin, Sztejnberg & Marder, ; Falk, Gadoury, Pearson & Seem, ).…”

“…This variation in resistance shapes the strength of epidemics at the local scale in nature and, in turn, affects the metapopulation dynamics of the pathogen (Jousimo et al., ; Susi & Laine, ). Podosphaera plantaginis is also subject to frequent attack by the fungal hyperparasite Ampelomyces (Parratt, Barres, Penczykowski & Laine, ), and previous work has found a negative impact of hyperparasitism on pathogen overwinter survival (Tollenaere et al., ). To date, there is some evidence that Ampelomyces mycoparasites inhibit growth and transmission of other powdery mildew species (Kiss et al., ), and thus represent a putative source of top‐down control on Po.…”

“…Indeed, the most robust evidence for such a phenomenon comes from studies of parasitoids and hyperparasitoids (e.g., Schooler, de Barro & Ives, 2011), organisms that occupy an ecological niche somewhere between predators and true pathogens (Godfray, 1994), and the effects of predators on invertebrate plant pests (Schellhorn, Bianchi & Hsu, 2014). Some theoretical and mostly observational research supports the hypothesis that hyperparasite infection may influence pathogen population structure and dynamics (Andersen et al, 2012;Holt & Hochberg, 1998;Springer, Baines, Fulbright, Chansler & Jarosz, 2013;Tollenaere et al, 2014). Probably the best studied case is the hypovirulence-inducing mycovirus CHV-1, which infects the chestnut blight pathogen Cryphonectria parasitica.…”

GFP transformation sheds more light on a widespread mycoparasitic interaction

“…fungi that parasitize other fungi, are commonly found in most terrestrial ecosystems, the best known species being those that attack fungal plant pathogens [1][2][3][4] . A number of mycoparasites have been long studied and commercially utilized as biocontrol agents (BCAs) of crop pathogens 3,4 ; others have been in focus as components of natural multitrophic relationships 2,[5][6][7][8][9] . Direct observation of interfungal parasitic relationships is notoriously difficult at cellular or hyphal level, using classical light, scanning and transmission electron microscopy (LM, SEM and TEM) and other visualization methods 1,[10][11][12][13] .…”