Inferring the multi-host fitness landscape of endive necrotic mosaic virus from cross-inoculation experiments

Fitness landscapes offer a compact representation of adaptation, yet are rarely inferred from sparse multi-environment data. We present a Bayesian approach to infer an effective multi-host phenotypic fitness landscape from cross-inoculation assays by linking successful infection probabilities to Fisher's geometrical model and to an explicit decomposition of establishment routes. The model estimates (i) the distance matrix among host-specific phenotypic optima, (ii) target-host permissiveness through the widths of fitness peaks, (iii) target-specific differences in the efficiency with which phenotypic suitability translates into successful infection, and (iv) the conditional probabilities that successful infections are attributed to direct establishment, rescue from standing variation in the source inoculum, or de novo rescue in the target host. We apply the approach to an experimental evolution dataset for endive necrotic mosaic virus evolved on five Asteraceae hosts and challenged in a full cross-inoculation design. The inferred landscape can be visualized as a phenotypic map of the host community, revealing pronounced heterogeneity in target-host permissiveness and a geometry broadly concordant with host phylogeny. By grounding assay-derived distances in an explicit mechanistic model, the approach provides a parsimonious representation of multi-host constraints that can be used to discuss establishment barriers and potential springboard hosts in heterogeneous communities. More broadly, it offers a general method for inferring effective fitness landscapes from sparse multi-environment data.

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Publication Details

Journal
Genetics
Published
2026-10-29
DOI
https://doi.org/10.1093/genetics/iyag302
Primary Topic
Evolution and Genetic Dynamics
Type
article
Field-Weighted Citation Impact
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article

Inferring the multi-host fitness landscape of endive necrotic mosaic virus from cross-inoculation experiments

Samuel Soubeyrand, Julien J. Papaix, Raphaël Forien, Benoît Moury et al.
Genetics
Evolution and Genetic Dynamics
article

Inferring the multi-host fitness landscape of endive necrotic mosaic virus from cross-inoculation experiments

Samuel Soubeyrand, Julien J. Papaix, Raphaël Forien, Benoît Moury, Lionel Roques, Karine Berthier, Thomas Lenormand, Guillaume Martin
article en

Abstract

Fitness landscapes offer a compact representation of adaptation, yet are rarely inferred from sparse multi-environment data. We present a Bayesian approach to infer an effective multi-host phenotypic fitness landscape from cross-inoculation assays by linking successful infection probabilities to Fisher's geometrical model and to an explicit decomposition of establishment routes. The model estimates (i) the distance matrix among host-specific phenotypic optima, (ii) target-host permissiveness through the widths of fitness peaks, (iii) target-specific differences in the efficiency with which phenotypic suitability translates into successful infection, and (iv) the conditional probabilities that successful infections are attributed to direct establishment, rescue from standing variation in the source inoculum, or de novo rescue in the target host. We apply the approach to an experimental evolution dataset for endive necrotic mosaic virus evolved on five Asteraceae hosts and challenged in a full cross-inoculation design. The inferred landscape can be visualized as a phenotypic map of the host community, revealing pronounced heterogeneity in target-host permissiveness and a geometry broadly concordant with host phylogeny. By grounding assay-derived distances in an explicit mechanistic model, the approach provides a parsimonious representation of multi-host constraints that can be used to discuss establishment barriers and potential springboard hosts in heterogeneous communities. More broadly, it offers a general method for inferring effective fitness landscapes from sparse multi-environment data.

Genetics
Centre National de la Recherche Scientifique (FR), École Pratique des Hautes Études (FR), Université de Montpellier (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Centre d'Écologie Fonctionnelle et Évolutive (FR), Institut des Sciences de l'Evolution de Montpellier (FR), Biostatistique et processus spatiaux (FR), Institut de Recherche pour le Développement (FR), Pathologie végétale (FR)
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Openalex Percentile: Top 15%
Evolution and Genetic Dynamics
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