Neutral genetic structuring of pathogen populations during rapid adaptation

Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, "with" and "without" host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bottleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue "with" host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

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Publication Details

Journal
Journal of Heredity
Published
2024-08-05
DOI
https://doi.org/10.1093/jhered/esae036
Citations
3
Primary Topic
Wheat and Barley Genetics and Pathology
Type
article
Field-Weighted Citation Impact
1.80

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article

Neutral genetic structuring of pathogen populations during rapid adaptation

Aurélien Tellier, Méline Saubin, Solenn Stoeckel, Fabien Halkett
3 citations
Journal of Heredity
Wheat and Barley Genetics and Pathology
1.80
article

Neutral genetic structuring of pathogen populations during rapid adaptation

Aurélien Tellier, Méline Saubin, Solenn Stoeckel, Fabien Halkett
article en
3 citations

Abstract

Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, "with" and "without" host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bottleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue "with" host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

Journal of HeredityVol. 116(1)
CEA CESTA (FR), Université de Bordeaux (FR), Ifremer (FR), Institut Agro Rennes-Angers (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Interactions Arbres-Microorganismes (FR), UMR BIOdiversity, GEnes & Communities (FR), Institut de Génétique, Environnement et Protection des Plantes (FR), L'Institut Agro (FR), Université de Rennes (FR), Technical University of Munich (DE), Université de Lorraine (FR)
Agence Nationale de la Recherche, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Responsible consumption and production
Openalex Percentile: Top 13%
Wheat and Barley Genetics and Pathology
1.80
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