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

Parratt, Steven R.; Barrès, Benoît; Penczykowski, Rachel M.; Laine, Anna‐Liisa

doi:10.1111/mec.13928

Cited by 23 publications

(21 citation statements)

References 76 publications

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“…Furthermore, in this study, we only present allopatric combinations of pathogen and hyperparasites collected from the same limited geographical area of 50 × 70 km, to control for any effect of local adaptation. In a previous study, we detailed that the outcome of hyperparasite infection can be significantly controlled by a specific genotype × genotype interactions (Parratt et al., ), so further exploration of any top‐down control with sympatric as well as allopatric combinations may reveal a stronger effect.…”

Section: Discussionsupporting

confidence: 91%

“…Podosphaera plantaginis is host to the hyperparasite Ampelomyces spp., a species complex of fungi found infecting powdery mildew species worldwide (Kiss et al., ). 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., ).…”

Section: Methodsmentioning

confidence: 99%

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

Parratt

Laine

2018

Journal of Applied Ecology

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The relative importance of bottom‐up versus top‐down control of population dynamics has been the focus of much debate. In infectious disease biology, research is typically focused on the bottom‐up process of host resistance, wherein the direction of control flows from the lower to the higher trophic level to impact on pathogen population size and epidemiology. However, the importance of top‐down control by a pathogen's natural enemies has been mostly overlooked.Here, we explore the effects of, and interaction between, host genotype (i.e., genetic susceptibility to pathogen infection) and infection by a hyperparasitic fungus, Ampelomyces spp., on the establishment and early epidemic growth and transmission of a powdery mildew plant pathogen (Podosphaera plantaginis). We used a semi‐natural field experiment to contrast the impacts of hyperparasite infection, host‐plant resistance and spatial structure to reveal the key factors that determine pathogen spread. We then used a laboratory‐based inoculation approach to test whether the field experiment results hold across multiple pathogen–host genetic combinations and to explore hyperparasite effects on the pathogen's later life‐history stages.We found that hyperparasite infection had a negligible effect on within‐host infection development and between‐host spread of the pathogen during the onset of epidemics. In contrast, host‐plant resistance was the major determinant of whether plants became infected, and host genotype and proximity to an infection source determined infection severity.Our laboratory study showed that, while the interaction between host and pathogen genotypes was the key determinant of infection outcome, hyperparasitism did, on average, reduce the severity of infection. Moreover, hyperparasite infection negatively influenced the production of the pathogen's overwintering structures. Synthesis and applications. Our results suggest that bottom‐up host resistance affects pathogen spread, but top‐down control of powdery mildew pathogens is likely more effective against later life‐history stages. Further, while hyperparasitism in this system can reduce early pathogen growth under stable laboratory conditions, this effect is not detectable in a semi‐natural environment. Considering the effects of hyperparasites at multiple points in pathogen's life history will be important when considering hyperparasite‐derived biocontrol measures in other natural and agricultural systems.

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Section: Discussionsupporting

confidence: 91%

Section: Methodsmentioning

confidence: 99%

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

Parratt

Laine

2018

Journal of Applied Ecology

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“…Plant Mini Kit (Omega Bio‐Tek, Norcross, GA, USA) at the Institute of Biotechnology, University of Helsinki. Samples were genotyped at 19 single nucleotide polymorphism (SNP) loci with the Sequenom iPlex platform at the Institute for Molecular Medicine Finland (Tollenaere et al ., ; Parratt et al ., ). Because P. plantaginis conidial spores are haploid, samples were classified as coinfected if two alleles were present at any locus (Tollenaere et al ., ).…”

Section: Methodsmentioning

confidence: 98%

“…for Molecular Medicine Finland (Tollenaere et al, 2012;Parratt et al, 2016a). Because P. plantaginis conidial spores are haploid, samples were classified as coinfected if two alleles were present at any locus (Tollenaere et al, 2012).…”

Section: Single Nucleotide Polymorphism Genotyping Of Pathogen Strainsmentioning

confidence: 99%

Effect of spatial connectivity on host resistance in a highly fragmented natural pathosystem

Höckerstedt

Sirén

Laine

2018

J of Evolutionary Biology

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Both theory and experimental evolution studies predict migration to influence the outcome of antagonistic coevolution between hosts and their parasites, with higher migration rates leading to increased diversity and evolutionary potential. Migration rates are expected to vary in spatially structured natural pathosystems, yet how spatial structure generates variation in coevolutionary trajectories across populations occupying the same landscape has not been tested. Here, we studied the effect of spatial connectivity on host evolutionary potential in a natural pathosystem characterized by a stable Plantago lanceolata host network and a highly dynamic Podosphaera plantaginis parasite metapopulation. We designed a large inoculation experiment to test resistance of five isolated and five well‐connected host populations against sympatric and allopatric pathogen strains, over 4 years. Contrary to our expectations, we did not find consistently higher resistance against sympatric pathogen strains in the well‐connected populations. Instead, host local adaptation varied considerably among populations and through time with greater fluctuations observed in the well‐connected populations. Jointly, our results suggest that in populations where pathogens have successfully established, they have the upper hand in the coevolutionary arms race, but hosts may be better able to respond to pathogen‐imposed selection in the well‐connected than in the isolated populations. Hence, the ongoing and extensive fragmentation of natural habitats may increase vulnerability to diseases.

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“…Few examples of obligate hyperparasites among fungi, however, have been well studied. Questions arise about what appears at first glance to be a risky lifestyle (Parratt, Barrès, Penczykowski, & Laine, ). How did such associations evolve?…”

Section: Introductionmentioning

confidence: 99%

Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations

Haelewaters

Page

Pfister

2018

Ecology and Evolution

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The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position‐induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.

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

Cited by 23 publications

References 76 publications

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

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

Effect of spatial connectivity on host resistance in a highly fragmented natural pathosystem

Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations

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