Section: Evolutionary Biology
Topic: Evolution, Microbiology, Plant biology
How to survive the mutational meltdown: lessons from plant RNA viruses
10.24072/pcjournal.379 - Peer Community Journal, Volume 4 (2024), article no. e22.
Get full text PDF Peer reviewed and recommended by PCI
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.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_379,
author = {Lafforgue, Guillaume and Lefebvre, Marie and Michon, Thierry and Elena, Santiago F.},
title = {How to survive the mutational meltdown: lessons from plant {RNA} viruses},
journal = {Peer Community Journal},
eid = {e22},
publisher = {Peer Community In},
volume = {4},
year = {2024},
doi = {10.24072/pcjournal.379},
language = {en},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.379/}
}
TY - JOUR AU - Lafforgue, Guillaume AU - Lefebvre, Marie AU - Michon, Thierry AU - Elena, Santiago F. TI - How to survive the mutational meltdown: lessons from plant RNA viruses JO - Peer Community Journal PY - 2024 VL - 4 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.379/ DO - 10.24072/pcjournal.379 LA - en ID - 10_24072_pcjournal_379 ER -
%0 Journal Article %A Lafforgue, Guillaume %A Lefebvre, Marie %A Michon, Thierry %A Elena, Santiago F. %T How to survive the mutational meltdown: lessons from plant RNA viruses %J Peer Community Journal %D 2024 %V 4 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.379/ %R 10.24072/pcjournal.379 %G en %F 10_24072_pcjournal_379
Lafforgue, Guillaume; Lefebvre, Marie; Michon, Thierry; Elena, Santiago F. How to survive the mutational meltdown: lessons from plant RNA viruses. Peer Community Journal, Volume 4 (2024), article no. e22. doi : 10.24072/pcjournal.379. https://peercommunityjournal.org/articles/10.24072/pcjournal.379/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100702
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Allele fixation in a dynamic metapopulation: Founder effects vs refuge effects, Theor Popul Biol, Volume 76 (2009), pp. 105-117 | DOI
[2] Analysis of genetic bottlenecks during horizontal transmission of cucumber mosaic virus, J Virol, Volume 80 (2006), pp. 8345-8350 | DOI
[3] Muller’s ratchet decreases fitness of a DNA-based microbe, Proc Natl Acad Sci USA, Volume 93 (1996), pp. 906-907 | DOI
[4] Adaptive evolution of asexual populations under Muller’s ratchet, Evolution, Volume 58 (2004), pp. 1403-1413 | DOI
[5] Genotypic but not phenotypic historical contingency revealed by viral experimental evolution, BMC Evol Biol, Volume 13 (2013) no. 46 | DOI
[6] Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus, J Virol, Volume 82 (2008), pp. 12416-12421 | DOI
[7] Sequential Bottlenecks Drive Viral Evolution in Early Acute Hepatitis C Virus Infection, PLoS Pathogens, Volume 7 (2011) no. 9 | DOI
[8] Distribution of fitness and virulence effects caused by single-nucleotide substitutions in tobacco etch virus, J Virol, Volume 81 (2007), pp. 12979-12984 | DOI
[9] Beneficial effects of population bottlenecks in an RNA virus evolving at increased error rate, J Mol Biol, Volume 384 (2008), pp. 1120-1129 | DOI
[10] Genetic variation in fitness within a clonal population of a plant RNA virus, Virus Evolution, Volume 2 (2016) no. 1 | DOI
[11] Fitness of RNA virus decreased by Muller’s ratchet, Nature, Volume 348 (1990), pp. 454-455 | DOI
[12] Effect of route of inoculation on experimental respiratory viral disease in volunteers and evidence for airborne transmission, Bacteriol Rev, Volume 30 (1966), pp. 517-529 | DOI
[13] Fate of a mutation in a fluctuating environment, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 36 | DOI
[14] Fitness Declines in Tobacco Etch Virus upon Serial Bottleneck Transfers, Journal of Virology, Volume 81 (2007) no. 10, pp. 4941-4947 | DOI
[15] Tagging of plant potyvirus replication and movement by insertion of beta-glucuronidase into the viral polyprotein., Proceedings of the National Academy of Sciences, Volume 89 (1992) no. 21, pp. 10208-10212 | DOI
[16] Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet., Proceedings of the National Academy of Sciences, Volume 89 (1992) no. 13, pp. 6015-6019 | DOI
[17] The evolution of viruses in multi-host fitness landscapes, Open Virol J, Volume 3 (2009), pp. 1-6 | DOI
[18] The evolutionary genetics of emerging plant RNA viruses, Mol Plant Microbe Interact, Volume 24 (2011), pp. 287-293 | DOI
[19] Evolutionary dynamics of fitness recovery from the debilitating effects of Muller’s ratchet, Evolution, Volume 52 (1998), pp. 309-314 | DOI
[20] Evolution of fitness in experimental populations of vesicular stomatitis virus, Genetics, Volume 142 (1996), pp. 673-679 | DOI
[21] Adaptive value of high mutation rates of RNA viruses: separating causes from consequences, J Virol, Volume 79 (2005), pp. 11555-11558 | DOI
[22] Genetic lesions associated with Muller’s ratchet in an RNA virus, J Mol Biol, Volume 264 (1996), pp. 255-267 | DOI
[23] Narrow Bottlenecks Affect Pea Seedborne Mosaic Virus Populations during Vertical Seed Transmission but not during Leaf Colonization, PLoS Pathogens, Volume 10 (2014) no. 1 | DOI
[24] Vertical Transmission of Hepatitis C Virus: Variable Transmission Bottleneck and Evidence of Midgestation In Utero Infection, Journal of Virology, Volume 91 (2017) no. 23 | DOI
[25] The evolutionary advantage of recombination, Genetics, Volume 78 (1974), pp. 737-756 | DOI
[26] Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching, Cell Host Microbe, Volume 19 (2016), pp. 481-492 | DOI
[27] Circulating Virus Load Determines the Size of Bottlenecks in Viral Populations Progressing within a Host, PLoS Pathogens, Volume 8 (2012) no. 11 | DOI
[28] The accumulation of deleterious genes in a population-Muller’s Ratchet, Theor Popul Biol, Volume 14 (1978), pp. 251-267 | DOI
[29] Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages, Virology, Volume 282 (2001), pp. 230-236 | DOI
[30] How to survive the mutational meltdown: lessons from plant RNA viruses, Peer Community in Evolutionary Biology (2024) | DOI
[31] Muller’s ratchet under epistatic selection, Genetics, Volume 136 (1994), pp. 1469-1473 | DOI
[32] Population variation of two viruses, Zenodo, 2023 | DOI
[33] Dynamics of the establishment of systemic potyvirus infection: independent yet cumulative action of primary infection sites, J Virol, Volume 86 (2012), pp. 12912-12922 | DOI
[34] Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus, Heredity, Volume 109 (2012), pp. 71-77 | DOI
[35] Effect of Host Species on the Distribution of Mutational Fitness Effects for an RNA Virus, PLoS Genetics, Volume 7 (2011) no. 11 | DOI
[36] Local lesions and induced resistance, Adv Virus Res, Volume 75 (2009), pp. 73-117 | DOI
[37] The mutational meltdown in asexual populations, J Heredity, Volume 84 (1993), pp. 339-344 | DOI
[38] The rate and character of spontaneous mutation in an RNA virus, Genetics, Volume 162 (2002), pp. 1505-1511 | DOI
[39] High mutation rates, bottlenecks, and robustness of RNA viral quasispecies, Gene, Volume 347 (2005), pp. 273-282 | DOI
[40] Why are viral genomes so fragile? The bottleneck hypothesis, PLOS Computational Biology, Volume 17 (2021) no. 7 | DOI
[41] Estimation of the size of genetic bottlenecks in cell-to-cell movement of soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements, J Virol, Volume 84 (2010), pp. 1828-1837 | DOI
[42] Large Bottleneck Size in Cauliflower Mosaic Virus Populations during Host Plant Colonization, PLoS Pathogens, Volume 4 (2008) no. 10 | DOI
[43] Estimation of the number of virus particles transmitted by an insect vector, Proc Natl Acad Sci USA, Volume 104 (2007), pp. 17891-17896 | DOI
[44] The relation of recombination to mutational advance, Mut Res, Volume 106 (1964), pp. 2-9 | DOI
[45] Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness, Journal of Virology, Volume 69 (1995) no. 5, pp. 2869-2872 | DOI
[46] Exponential increases of RNA virus fitness during large population transmissions, Proc Natl Acad Sci USA, Volume 92 (1995), pp. 5841-5844 | DOI
[47] A ruby in the rubbish; beneficial mutations, deleterious mutations and the evolution of sex, Genetics, Volume 137 (1994), pp. 597-606 | DOI
[48] Complexities of Viral Mutation Rates, Journal of Virology, Volume 92 (2018) no. 14 | DOI
[49] Bottleneck-mediated quasispecies restriction during spread of an RNA virus from inoculation site to brain, Proc Natl Acad Sci USA, Volume 103 (2006), pp. 5520-5525 | DOI
[50] Helper-dependent vector transmission of plant viruses, Annu Rev Phytopathol, Volume 34 (1996), pp. 227-247 | DOI
[51] Estimation of population bottlenecks during systemic movement of tobacco mosaic virus in tobacco plants, J Virol, Volume 77 (2003), pp. 9906-9911 | DOI
[52] Mechanisms of viral mutation, Cell Mol Life Sci, Volume 73 (2016), pp. 4433-4448 | DOI
[53] Viral mutation rates, J Virol, Volume 84 (2010), pp. 9733-9748 | DOI
[54] Transmission modes affect the population structure of potato virus Y in potato, PLOS Pathogens, Volume 16 (2020) no. 6 | DOI
[55] Zucchini yellow mosaic virus (ZYMV, Potyvirus): Vertical transmission, seed infection and cryptic infections, Virus Res, Volume 176 (2013), pp. 259-264 | DOI
[56] Slowly switching between environments facilitates reverse evolution in small populations, Evolution, Volume 66 (2012), pp. 3144-3154 | DOI
[57] The rate and spectrum of spontaneous mutations in a plant RNA virus, Genetics, Volume 185 (2010), pp. 983-989 | DOI
[58] Estimation of the in vivo recombination rate for a plant RNA virus, J Gen Virol, Volume 95 (2014), pp. 724-732 | DOI
[59] Within-Host Spatiotemporal Dynamics of Plant Virus Infection at the Cellular Level, PLoS Genetics, Volume 10 (2014) no. 2 | DOI
[60] Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species, PLoS Pathogens, Volume 7 (2011) no. 5 | DOI
[61] Evolution in mendelian populations, Genetics, Volume 16 (1931), pp. 97-159 | DOI
[62] Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events, J Virol, Volume 73 (1999), pp. 2745-2751 | DOI
[63] Mutational meltdown in laboratory yeast populations, Evolution, Volume 55 (2001), pp. 909-917 | DOI
[64] Matters of size: genetic bottlenecks in virus infection and their potential impact on evolution, Annu Rev Virol, Volume 2 (2015), pp. 161-179 | DOI
[65] One Is Enough: In Vivo Effective Population Size Is Dose-Dependent for a Plant RNA Virus, PLoS Pathogens, Volume 7 (2011) no. 7 | DOI
[66] An experimental test of the independent action hypothesis in virus–insect pathosystems, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1665, pp. 2233-2242 | DOI
[67] Heterogeneous Host Susceptibility Enhances Prevalence of Mixed-Genotype Micro-Parasite Infections, PLoS Computational Biology, Volume 7 (2011) no. 6 | DOI
Cited by Sources: