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Spatial variation in disease resistance: from molecules to metapopulations.

ABSTRACT: Variation in disease resistance is a widespread phenomenon in wild plant-pathogen associations. Here, we review current literature on natural plant-pathogen associations to determine how diversity in disease resistance is distributed at different hierarchical levels - within host individuals, within host populations, among host populations at the metapopulation scale and at larger regional scales.We find diversity in resistance across all spatial scales examined. Furthermore, variability seems to be the best counter-defence of plants against their rapidly evolving pathogens. We find that higher diversity of resistance phenotypes also results in higher levels of resistance at the population level.Overall, we find that wild plant populations are more likely to be susceptible than resistant to their pathogens. However, the degree of resistance differs strikingly depending on the origin of the pathogen strains used in experimental inoculation studies. Plant populations are on average 16% more resistant to allopatric pathogen strains than they are to strains that occur within the same population (48 % vs. 32 % respectively).Pathogen dispersal mode affects levels of resistance in natural plant populations with lowest levels detected for hosts of airborne pathogens and highest for waterborne pathogens.Detailed analysis of two model systems, Linum marginale infected by Melampsora lini, and Plantago lanceolata infected by Podosphaera plantaginis, show that the amount of variation in disease resistance declines towards higher spatial scales as we move from individual hosts to metapopulations, but evaluation of multiple spatial scales is needed to fully capture the structure of disease resistance.Synthesis: Variation in disease resistance is ubiquitous in wild plant-pathogen associations. While the debate over whether the resistance structure of plant populations is determined by pathogen-imposed selection versus non-adaptive processes remains unresolved, we do report examples of pathogen-imposed selection on host resistance. Here we highlight the importance of measuring resistance across multiple spatial scales, and of using sympatric strains when looking for signs of coevolution in wild plant-pathogen interactions.

SUBMITTER: Laine AL

PROVIDER: S-EPMC3020101 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Spatial variation in disease resistance: from molecules to metapopulations.

Laine Anna-Liisa AL Burdon Jeremy J JJ Dodds Peter N PN Thrall Peter H PH

Journal of Ecology. 20110101 1

Variation in disease resistance is a widespread phenomenon in wild plant-pathogen associations. Here, we review current literature on natural plant-pathogen associations to determine how diversity in disease resistance is distributed at different hierarchical levels - within host individuals, within host populations, among host populations at the metapopulation scale and at larger regional scales.We find diversity in resistance across all spatial scales examined. Furthermore, variability seems t ...[more]

PMID: 21243068

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Project description:The mass release of transgenic insects carrying female lethal self-limiting genes can reduce pest insect populations. Substantial releases are also a novel resistance management tool, since wild type alleles conferring susceptibility to pesticides can dilute resistance alleles in target populations. However, a potential barrier is the need for large-scale area-wide releases. Here, we address whether localized releases of transgenic insects could provide an alternative means of population suppression and resistance management, without serious loss of efficacy.We used experimental mesocosms constituting insect metapopulations to explore the evolution of resistance to the Bacillus thuringiensis toxin Cry1Ac in a high-dose/refugia landscape in the insect Plutella xylostella. We ran two selection experiments, the first compared the efficacy of "everywhere" releases and negative controls to a spatially density-dependent or "whack-a-mole" strategy that concentrated release of transgenic insects in subpopulations with elevated resistance. The second experiment tested the relative efficacy of whack-a-mole and everywhere releases under spatially homogenous and heterogeneous selection pressure.The whack-a-mole releases were less effective than everywhere releases in terms of slowing the evolution of resistance, which, in the first experiment, largely prevented the evolution of resistance. In contrast to predictions, heterogeneous whack-a-mole releases were no more effective under heterogeneous selection pressure. Heterogeneous selection pressure did, however, reduce total insect population sizes.Whack-a-mole releases provided early population suppression, indistinguishable from homogeneous everywhere releases. However, insect population densities tracked the evolution of resistance in this system, as phenotypic resistance provides access to additional diet containing the toxin Cry1Ac. Thus, as resistance levels diverged between treatments, carrying capacities and population sizes increased under the whack-a-mole approach. Synthesis and applications. Spatially density-dependent releases of transgenic insects, particularly those targeting source populations at a landscape level, could suppress pest populations in the absence of blanket area-wide releases. The benefits of self-limiting transgenic insects were reduced in spatially localized releases, suggesting that they are not ideal for "spot" treatment of resistance problems. Nevertheless, spatially homogeneous or heterogeneous releases could be used to support other resistance management interventions.

Project description:BackgroundThe development of insecticide resistance in disease-vectoring mosquito species can lead to vector control failure and disease resurgence. However, insecticide applications remain an essential public health intervention. In Florida, insecticide resistance in Aedes aegypti, an anthropophilic mosquito species capable of transmitting dengue, chikungunya, and Zika virus, is a major concern. Understanding the location, scale, and driving factors of insecticide resistance can enhance the ability of vector control organizations to target populations effectively.MethodsWe used previously collected data on frequencies of mutations that confer resistance to commonly used pyrethroid insecticides in Ae. aegypti specimens from 62 sites distributed across 18 counties in Florida. To determine the scale of clustering for the most resistant variant, we used a Ripley's K function. We also used a spatial scanning statistic technique to identify locations of clusters where higher than expected frequencies of susceptible or resistant mosquitoes occurred. We then tested for associations between landscape, demographic, and insecticide-use factors using a beta regression modelling approach and evaluated the effect of spatial lag and spatial error terms on overall explanatory power of these models.ResultsThe scale at which maximum clustering of the most resistant variant occurs is approximately 20 kilometers. We identified statistically significant clusters of genotypes associated with resistance in several coastal cities, although some of these clusters were near significant clusters of susceptible mosquitoes, indicating selection pressures vary at the local scale. Vegetation density, distance from roads, and pyrethroid-use by vector control districts were consistently significant predictors of knockdown resistance genotype frequency in the top-performing beta regression models, although pyrethroid use surprisingly had a negatively associated with resistance. The incorporation of spatial lags resulted in improvements to the fit and explanatory power of the models, indicating an underlying diffusion process likely explains some of the spatial patterns observed.ConclusionsThe genetic mutations that confer resistance to pyrethroids in Ae. aegypti mosquitoes in Florida exhibit spatial autocorrelation and patterns that can be partially explained by landscape and insecticide-use factors. Further work at local scales should be able to identify the mechanisms by which these variables influence selection for alleles associated with resistance.

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Spatial variation in disease resistance: from molecules to metapopulations.

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Spatial variation in disease resistance: from molecules to metapopulations.

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