Evolutionary Epidemiology of Drug-Resistance in Space

Débarre, Florence; Lenormand, Thomas; Gandon, Sylvain

doi:10.1371/journal.pcbi.1000337

Cited by 30 publications

(37 citation statements)

References 50 publications

(48 reference statements)

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“…A key point is that, in heterogeneous environments, adaptation and range expansion are likely coupled. This fundamentally distinguishes the staircase model from other models with spatially structured populations (31)(32)(33)(34)(35)(36), or models of evolution at the front of growing colonies (37). This has important consequences.…”

Section: Discussionmentioning

confidence: 99%

On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient

Hermsen

Deris

Hwa

2012

Proc. Natl. Acad. Sci. U.S.A.

175

216

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The rapid emergence of bacterial strains resistant to multiple antibiotics is posing a growing public health risk. The mechanisms underlying the rapid evolution of drug resistance are, however, poorly understood. The heterogeneity of the environments in which bacteria encounter antibiotic drugs could play an important role. E.g., in the highly compartmentalized human body, drug levels can vary substantially between different organs and tissues. It has been proposed that this could facilitate the selection of resistant mutants, and recent experiments support this. To study the role of spatial heterogeneity in the evolution of drug resistance, we present a quantitative model describing an environment subdivided into relatively isolated compartments with various antibiotic concentrations, in which bacteria evolve under the stochastic processes of proliferation, migration, mutation and death. Analytical and numerical results demonstrate that concentration gradients can foster a mode of adaptation that is impossible in uniform environments. It allows resistant mutants to evade competition and circumvent the slow process of fixation by invading compartments with higher drug concentrations, where less resistant strains cannot subsist. The speed of this process increases sharply with the sensitivity of the growth rate to the antibiotic concentration, which we argue to be generic. Comparable adaptation rates in uniform environments would require a high selection coefficient (s > 0.1) for each forward mutation. Similar processes can occur if the heterogeneity is more complex than just a linear gradient. The model may also be applicable to other adaptive processes involving environmental heterogeneity and range expansion.first passage processes | stochastic modeling | evolutionary ecology

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Section: Discussionmentioning

confidence: 99%

On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient

Hermsen

Deris

Hwa

2012

Proc. Natl. Acad. Sci. U.S.A.

175

216

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“…In addition, understanding transient evolutionary dynamics may also be particularly helpul to public health management. In particular, several attempts have been made to better understand the spread of drug resistance in spatially heterogeneous environments (Débarre et al., ). Generalizing those studies to a broader range of epidemiological scenarios would help identify strategies that limit or even prevent the spread of drug resistance in spatially structured environments.…”

Section: Perspectivesmentioning

confidence: 99%

Evolution of spatially structured host–parasite interactions

Lion

Gandon

2015

J of Evolutionary Biology

110

105

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Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host-parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life-history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host-parasite life cycle and on which life-history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host-parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.

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“…We also assumed that the five main pathotypes considered in the study were pre-existing and homogeneously distributed at the country scale. Theoretical models predict that local structures in the host population could be crucial in the invasion dynamics of pathogens (Keeling, 1999;Park et al, 2001;Débarre et al, 2009). A possible improvement of the analysis would be to test whether weakening the assumption of complete mixing of the population at the national level would alter the results.…”

Section: Researchmentioning

confidence: 99%

Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics

et al. 2011

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Summary• In plant pathology, the idea of designing variety management strategies at the scale of cultivated landscapes is gaining more and more attention. This requires the identification of effects that take place at large scales on host and pathogen populations. Here, we show how the landscape varietal composition influences the resistance level (as measured in the field) of the most grown wheat varieties by altering the structure of the pathogen populations.• For this purpose, we jointly analysed three large datasets describing the wheat leaf rust pathosystem (Puccinia triticina ⁄ Triticum aestivum) at the country scale of France with a Bayesian hierarchical model.• We showed that among all compatible pathotypes, some were preferentially associated with a variety, that the pathotype frequencies on a variety were affected by the landscape varietal composition, and that the observed resistance level of a variety was linked to the frequency of the most aggressive pathotypes among all compatible pathotypes.• This data exploration establishes a link between the observed resistance level of a variety and landscape composition at the national scale. It illustrates that the quantitative aspects of the host-pathogen relationship have to be considered in addition to the major resistance ⁄ virulence factors in landscape epidemiology approaches.

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Evolutionary Epidemiology of Drug-Resistance in Space

Cited by 30 publications

References 50 publications

On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient

On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient

Evolution of spatially structured host–parasite interactions

Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics

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