How to survive the mutational meltdown: lessons from plant RNA viruses

Muller's ratchet refers to the irreversible accumulation of deleterious mutations in small populations, resulting in a decline in overall fitness. This phenomenon has been extensively observed in experiments involving microorganisms, including bacteriophages and yeast. While the impact of Mulle...

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Main Authors: Lafforgue, Guillaume, Lefebvre, Marie, Michon, Thierry, Elena, Santiago F.
Format: Article
Language:English
Published: Peer Community In 2024-02-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.379/
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author Lafforgue, Guillaume
Lefebvre, Marie
Michon, Thierry
Elena, Santiago F.
author_facet Lafforgue, Guillaume
Lefebvre, Marie
Michon, Thierry
Elena, Santiago F.
author_sort Lafforgue, Guillaume
collection DOAJ
description Muller's ratchet refers to the irreversible accumulation of deleterious mutations in small populations, resulting in a decline in overall fitness. This phenomenon has been extensively observed in experiments involving microorganisms, including bacteriophages and yeast. While the impact of Muller’s ratchet on viruses has been largely studied in bacteriophages and animal RNA viruses, its effects on plant RNA viruses remain poorly documented. Plant RNA viruses give rise to large and diverse populations that undergo significant bottlenecks during the colonization of distant tissues or through vector-mediated horizontal transmission. In this study, we aim to investigate the role of bottleneck size, the maximum population size between consecutive bottlenecks, and the generation of genetic diversity in countering the effects of Muller’s ratchet. We observed three distinct evolutionary outcomes for tobacco etch virus under three different demographic conditions: (i) a decline in fitness following periodic severe bottlenecks in Chenopodium quinoa, (ii) a consistent fitness level with moderate bottlenecks in C. quinoa, and (iii) a net increase in fitness when severe bottlenecks in C. quinoa were alternated with large population expansions in Nicotiana tabacum. By fitting empirical data to an in silico simulation model, we found that initiating a lesion in C. quinoa required only 1-5 virions, and approximately 40 new virions were produced per lesion. These findings demonstrate that Muller's ratchet can be halted not only by increasing the number of founder viruses but also by incorporating phases of exponential growth to large populations between bottlenecks. Such population expansions generate genetic diversity, serving as a buffer against, and potentially even leveraging, the effects of genetic drift.
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spelling doaj-art-910c1911b0874081a2a65dcbe78bf8ee2025-02-07T10:17:18ZengPeer Community InPeer Community Journal2804-38712024-02-01410.24072/pcjournal.37910.24072/pcjournal.379How to survive the mutational meltdown: lessons from plant RNA viruses Lafforgue, Guillaume0https://orcid.org/0000-0003-2215-2825Lefebvre, Marie1https://orcid.org/0000-0002-3093-5873Michon, Thierry2https://orcid.org/0000-0002-0041-9376Elena, Santiago F.3https://orcid.org/0000-0001-8249-5593UMR Biologie du Fruit et Pathologie, INRAE, Université de Bordeaux, Villenave d’Ornon, FranceUMR Biologie du Fruit et Pathologie, INRAE, Université de Bordeaux, Villenave d’Ornon, FranceUMR Biologie du Fruit et Pathologie, INRAE, Université de Bordeaux, Villenave d’Ornon, FranceInstituto de Biología Integrativa de Sistemas (I2SysBio), Consejo Superior de Investigaciones Científicas – Universitat de València, Paterna, 46980 València, Spain; The Santa Fe Institute, Santa Fe, NM 87501, USAMuller's ratchet refers to the irreversible accumulation of deleterious mutations in small populations, resulting in a decline in overall fitness. This phenomenon has been extensively observed in experiments involving microorganisms, including bacteriophages and yeast. While the impact of Muller’s ratchet on viruses has been largely studied in bacteriophages and animal RNA viruses, its effects on plant RNA viruses remain poorly documented. Plant RNA viruses give rise to large and diverse populations that undergo significant bottlenecks during the colonization of distant tissues or through vector-mediated horizontal transmission. In this study, we aim to investigate the role of bottleneck size, the maximum population size between consecutive bottlenecks, and the generation of genetic diversity in countering the effects of Muller’s ratchet. We observed three distinct evolutionary outcomes for tobacco etch virus under three different demographic conditions: (i) a decline in fitness following periodic severe bottlenecks in Chenopodium quinoa, (ii) a consistent fitness level with moderate bottlenecks in C. quinoa, and (iii) a net increase in fitness when severe bottlenecks in C. quinoa were alternated with large population expansions in Nicotiana tabacum. By fitting empirical data to an in silico simulation model, we found that initiating a lesion in C. quinoa required only 1-5 virions, and approximately 40 new virions were produced per lesion. These findings demonstrate that Muller's ratchet can be halted not only by increasing the number of founder viruses but also by incorporating phases of exponential growth to large populations between bottlenecks. Such population expansions generate genetic diversity, serving as a buffer against, and potentially even leveraging, the effects of genetic drift.https://peercommunityjournal.org/articles/10.24072/pcjournal.379/
spellingShingle Lafforgue, Guillaume
Lefebvre, Marie
Michon, Thierry
Elena, Santiago F.
How to survive the mutational meltdown: lessons from plant RNA viruses
Peer Community Journal
title How to survive the mutational meltdown: lessons from plant RNA viruses
title_full How to survive the mutational meltdown: lessons from plant RNA viruses
title_fullStr How to survive the mutational meltdown: lessons from plant RNA viruses
title_full_unstemmed How to survive the mutational meltdown: lessons from plant RNA viruses
title_short How to survive the mutational meltdown: lessons from plant RNA viruses
title_sort how to survive the mutational meltdown lessons from plant rna viruses
url https://peercommunityjournal.org/articles/10.24072/pcjournal.379/
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