Browse by volume Browse by section Browse by topic Browse by conference

Section: Evolutionary Biology
Topic: Evolution, Biology of interactions, Population biology

Experimental evolution of virulence and associated traits in a Drosophila melanogaster–Wolbachia symbiosis

Monnin, David1  ; Kremer, Natacha1 ; Michaud, Caroline1 ; Villa, Manon1; Henri, Hélène1 ; Desouhant, Emmanuel1 ; Vavre, Fabrice1 
1 Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69622 Villeurbanne, France

10.24072/pcjournal.9 - Peer Community Journal, Volume 1 (2021), article no. e9.

Get full text PDF Peer reviewed and recommended by PCI

Evolutionary theory predicts that vertically transmitted symbionts are selected for low virulence, as their fitness is directly correlated to that of their host. In contrast with this prediction, the Wolbachia strain wMelPop drastically reduces its Drosophila melanogaster host lifespan at high rearing temperatures. It is generally assumed that this feature is maintained because the D. melanogaster-wMelPop symbiosis is usually not exposed to environmental conditions in which the symbiont is virulent. To test this hypothesis, we submitted wMelPop-infected D. melanogaster lines to 17 generations of experimental evolution at a high temperature, while enforcing late reproduction by artificial selection. The fly survival was measured at different time points, as well as two traits that have been proposed to be causally responsible for wMelPop virulence: its relative density and the mean number of copies of octomom, an 8-genes region of the Wolbachia genome. We hypothesised that these conditions (high temperature and late reproduction) would select for a reduced wMelPop virulence, a reduced wMelPop density, and a reduced octomom copy number. Our results indicate that density, octomom copy number and virulence are correlated to each other. However, contrary to our expectations, we could not detect any reduction in virulence during the course of evolution. We discuss the significance of our results with respect to the evolutionary causes of wMelPop virulence.

Published online:
DOI: 10.24072/pcjournal.9
Type: Research article
Monnin, David 1; Kremer, Natacha 1; Michaud, Caroline 1; Villa, Manon 1; Henri, Hélène 1; Desouhant, Emmanuel 1; Vavre, Fabrice 1

1 Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69622 Villeurbanne, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_9,
     author = {Monnin, David and Kremer, Natacha and Michaud, Caroline and Villa, Manon and Henri, H\'el\`ene and Desouhant, Emmanuel and Vavre, Fabrice},
     title = {Experimental evolution of virulence and associated traits in a {\protect\emph{Drosophila} {melanogaster{\textendash}Wolbachia}} symbiosis},
     journal = {Peer Community Journal},
     eid = {e9},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.9},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.9/}
}
TY  - JOUR
AU  - Monnin, David
AU  - Kremer, Natacha
AU  - Michaud, Caroline
AU  - Villa, Manon
AU  - Henri, Hélène
AU  - Desouhant, Emmanuel
AU  - Vavre, Fabrice
TI  - Experimental evolution of virulence and associated traits in a Drosophila melanogaster–Wolbachia symbiosis
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.9/
DO  - 10.24072/pcjournal.9
ID  - 10_24072_pcjournal_9
ER  - 
%0 Journal Article
%A Monnin, David
%A Kremer, Natacha
%A Michaud, Caroline
%A Villa, Manon
%A Henri, Hélène
%A Desouhant, Emmanuel
%A Vavre, Fabrice
%T Experimental evolution of virulence and associated traits in a Drosophila melanogaster–Wolbachia symbiosis
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.9/
%R 10.24072/pcjournal.9
%F 10_24072_pcjournal_9
Monnin, David; Kremer, Natacha; Michaud, Caroline; Villa, Manon; Henri, Hélène; Desouhant, Emmanuel; Vavre, Fabrice. Experimental evolution of virulence and associated traits in a Drosophila melanogaster–Wolbachia symbiosis. Peer Community Journal, Volume 1 (2021), article  no. e9. doi : 10.24072/pcjournal.9. https://peercommunityjournal.org/articles/10.24072/pcjournal.9/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100111

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] Alizon, S.; de Roode, J. C.; Michalakis, Y. Multiple infections and the evolution of virulence, Ecology Letters, Volume 16 (2013) no. 4, pp. 556-567 | DOI

[2] ALIZON, S.; HURFORD, A.; MIDEO, N.; VAN BAALEN, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future, Journal of Evolutionary Biology, Volume 22 (2009) no. 2, pp. 245-259 | DOI

[3] Anderson, R. M.; May, R. M. Coevolution of hosts and parasites, Parasitology, Volume 85 (1982) no. 2, pp. 411-426 | DOI

[4] Bourtzis, K.; Nirgianaki, A.; Markakis, G.; Savakis, C. Wolbachia Infection and Cytoplasmic Incompatibility in Drosophila Species, Genetics, Volume 144 (1996) no. 3, pp. 1063-1073 | DOI

[5] Bull, J. J.; Molineux, I. J.; Rice, W. R. Selection of Benevolence in a Host-Parasite System, Evolution, Volume 45 (1991) no. 4 | DOI

[6] Bustin, S. A.; Benes, V.; Garson, J. A.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M. W.; Shipley, G. L.; Vandesompele, J.; Wittwer, C. T. The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments, Clinical Chemistry, Volume 55 (2009) no. 4, pp. 611-622 | DOI

[7] Chrostek, E.; Marialva, M. S. P.; Esteves, S. S.; Weinert, L. A.; Martinez, J.; Jiggins, F. M.; Teixeira, L. Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis, PLoS Genetics, Volume 9 (2013) no. 12 | DOI

[8] Chrostek, E.; Teixeira, L. Mutualism Breakdown by Amplification of Wolbachia Genes, PLOS Biology, Volume 13 (2015) no. 2 | DOI

[9] Chrostek, E.; Teixeira, L. Comment on Rohrscheib et al. 2016 "Intensity of mutualism breakdown is determined by temperature not amplification of Wolbachia genes", PLOS Pathogens, Volume 13 (2017) no. 9 | DOI

[10] Chrostek, E.; Teixeira, L. Within host selection for faster replicating bacterial symbionts, PLOS ONE, Volume 13 (2018) no. 1 | DOI

[11] Clancy, D. J.; Hoffmann, A. A. Behavior ofWolbachiaEndosymbionts FromDrosophila SimulansinDrosophila Serrata, A Novel Host, The American Naturalist, Volume 149 (1997) no. 5, pp. 975-988 | DOI

[12] David JR, C. M. Interaction entre le génotype et le milieu d’élevage. Conséquences sur les caractéristiques du développement de la Drosophile, Bulletin Biologique de la France et de la Belgique, Volume 99 (1965)

[13] Duarte, E. H.; Carvalho, A.; López-Madrigal, S.; Costa, J.; Teixeira, L. Forward genetics in Wolbachia: Regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island, PLOS Genetics, Volume 17 (2021) no. 6 | DOI

[14] Ewald, P. W. Host-Parasite Relations, Vectors, and the Evolution of Disease Severity, Annual Review of Ecology and Systematics, Volume 14 (1983) no. 1, pp. 465-485 | DOI

[15] Giordano, R.; O'Neill, S. L.; Robertson, H. M. Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana., Genetics, Volume 140 (1995) no. 4, pp. 1307-1317 | DOI

[16] Hoffmann, A. A.; Clancy, D. J.; Merton, E. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster., Genetics, Volume 136 (1994) no. 3, pp. 993-999 | DOI

[17] Hoffmann, A. A.; Turelli, M.; Harshman, L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans., Genetics, Volume 126 (1990) no. 4, pp. 933-948 | DOI

[18] Hoffmann, A. A.; Hercus, M.; Dagher, H. Population Dynamics of the Wolbachia Infection Causing Cytoplasmic Incompatibility in Drosophila melanogaster, Genetics, Volume 148 (1998) no. 1, pp. 221-231 | DOI

[19] Mazzucco, R.; Nolte, V.; Vijayan, T.; Schlötterer, C. Long-Term Dynamics Among Wolbachia Strains During Thermal Adaptation of Their Drosophila melanogaster Hosts, Frontiers in Genetics, Volume 11 (2020) | DOI

[20] McGraw, E. A.; Merritt, D. J.; Droller, J. N.; O'Neill, S. L. Wolbachia density and virulence attenuation after transfer into a novel host, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 5, pp. 2918-2923 | DOI

[21] Messenger, S. L.; Molineux, I. J.; Bull, J. J. Virulence evolution in a virus obeys a trade off, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 266 (1999) no. 1417, pp. 397-404 | DOI

[22] Min, K.-T.; Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death, Proceedings of the National Academy of Sciences, Volume 94 (1997) no. 20, pp. 10792-10796 | DOI

[23] Mira, A.; Moran, N. Estimating Population Size and Transmission Bottlenecks in Maternally Transmitted Endosymbiotic Bacteria, Microbial Ecology, Volume 44 (2002) no. 2, pp. 137-143 | DOI

[24] Monnin, D.; Kremer, N.; Berny, C.; Henri, H.; Dumet, A.; Voituron, Y.; Desouhant, E.; Vavre, F. Influence of oxidative homeostasis on bacterial density and cost of infection in Drosophila -Wolbachia symbioses, Journal of Evolutionary Biology, Volume 29 (2016) no. 6, pp. 1211-1222 | DOI

[25] Poinsot, D.; Merçot, H. WOLBACHIA INFECTION IN DROSOPHILA SIMULANS : DOES THE FEMALE HOST BEAR A PHYSIOLOGICAL COST?, Evolution, Volume 51 (2014) no. 1, pp. 180-186 | DOI

[26] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/., 2016

[27] Reynolds, K. T.; Thomson, L. J.; Hoffmann, A. A. The Effects of Host Age, Host Nuclear Background and Temperature on Phenotypic Effects of the Virulent Wolbachia Strain popcorn in Drosophila melanogaster, Genetics, Volume 164 (2003) no. 3, pp. 1027-1034 | DOI

[28] Rohrscheib, C. E.; Frentiu, F. D.; Horn, E.; Ritchie, F. K.; van Swinderen, B.; Weible, M. W.; O’Neill, S. L.; Brownlie, J. C. Response to: Comment on Rohrscheib et al. 2016 "Intensity of mutualism breakdown is determined by temperature not amplification of Wolbachia genes", PLOS Pathogens, Volume 13 (2017) no. 9 | DOI

[29] Al-Hatmi, A. M. S.; Meis, J. F.; de Hoog, G. S. Fusarium: Molecular Diversity and Intrinsic Drug Resistance, PLOS Pathogens, Volume 12 (2016) no. 4 | DOI

[30] Stewart, A. D.; Logsdon, J. M.; Kelley, S. E. AN EMPIRICAL STUDY OF THE EVOLUTION OF VIRULENCE UNDER BOTH HORIZONTAL AND VERTICAL TRANSMISSION, Evolution, Volume 59 (2005) no. 4, pp. 730-739 | DOI

[31] Strunov, A.; Kiseleva, E.; Gottlieb, Y. Spatial and temporal distribution of pathogenic Wolbachia strain wMelPop in Drosophila melanogaster central nervous system under different temperature conditions, Journal of Invertebrate Pathology, Volume 114 (2013) no. 1, pp. 22-30 | DOI

[32] Turelli, M.; Hoffmann, A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations., Genetics, Volume 140 (1995) no. 4, pp. 1319-1338 | DOI

[33] Turner, P. E.; Cooper, V. S.; Lenski, R. E. Tradeoff Between Horizontal and Vertical Modes of Transmission in Bacterial Plasmids, Evolution, Volume 52 (1998) no. 2 | DOI

Cited by Sources: