Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics

Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors

10.24072/pcjournal.50 - Peer Community Journal, Volume 1 (2021), article no. e38.

Get full text PDF Peer reviewed and recommended by PCI

Symbiosis is a continuum of long-term interactions ranging from mutualism to parasitism, according to the balance between costs and benefits for the protagonists. The density of endosymbionts is, in both cases, a key factor that determines both the transmission of symbionts and the host extended phenotype, and is thus tightly regulated within hosts. However, the evolutionary and molecular mechanisms underlying bacterial density regulation are currently poorly understood. In this context, the symbiosis between the fruit fly and its intracellular bacteria Wolbachia (wMelPop strain) is particularly interesting to study. Although vertically transmitted, the symbiont is pathogenic, and a positive correlation between virulence and wMelPop density is observed. In addition, the number of repeats of a bacterial genomic region -Octomom- is positively correlated with Wolbachia density, underlying a potential genetic mechanism that controls bacterial density. Interestingly, the number of repeats varies between host individuals, but most likely also within them. Such genetic heterogeneity within the host could promote conflicts between bacteria themselves and with the host, notably by increasing within-host competition between symbiont genotypes through a process analogous to the tragedy of the commons. To characterize the determinisms at play in the regulation of bacterial density, we first introgressed wMelPop in different genetic backgrounds of D. melanogaster, and found different density levels and Octomom copy numbers in each host lineage. To determine whether such variations reflect a host genetic determinism on density regulation through Octomom copy number selection, we replicated the introgressions and performed reciprocal crosses on the two Drosophila populations with the most extreme density levels. In both experiments, we detected an absence of directionality in the patterns of infection, associated with a strong instability of these patterns across generations. Given that bacterial density was highly correlated with Octomom copy numbers in all experiments, these results rather suggest a strong influence of drift and a random increase in the frequency of certain bacterial variants. We then discuss how drift, both on the symbiont population during transmission and on the host population, could limit the efficiency of selection in such a symbiotic system, and the consequences of drift on the regulation of density and composition of bacterial populations.

Published online:
DOI: 10.24072/pcjournal.50
Type: Research article
Bénard, Alexis 1; Henri, Hélène 1; Noûs, Camille 2; Vavre, Fabrice 1; Kremer, Natacha 1

1 Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
2 Laboratoire Cogitamus, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {B\'enard, Alexis and Henri, H\'el\`ene and No\^us, Camille and Vavre, Fabrice and Kremer, Natacha},
     title = {\protect\emph{Wolbachia} load variation in {\protect\emph{Drosophila}} is more likely caused by drift than by host genetic factors},
     journal = {Peer Community Journal},
     eid = {e38},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.50},
     url = {}
AU  - Bénard, Alexis
AU  - Henri, Hélène
AU  - Noûs, Camille
AU  - Vavre, Fabrice
AU  - Kremer, Natacha
TI  - Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.50
ID  - 10_24072_pcjournal_50
ER  - 
%0 Journal Article
%A Bénard, Alexis
%A Henri, Hélène
%A Noûs, Camille
%A Vavre, Fabrice
%A Kremer, Natacha
%T Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.50
%F 10_24072_pcjournal_50
Bénard, Alexis; Henri, Hélène; Noûs, Camille; Vavre, Fabrice; Kremer, Natacha. Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors. Peer Community Journal, Volume 1 (2021), article  no. e38. doi : 10.24072/pcjournal.50.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100126

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] Abbot, P.; Moran, N. A. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus), Molecular Ecology, Volume 11 (2002) no. 12, pp. 2649-2660 | 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 (2008) no. 2, pp. 245-259 | DOI

[3] 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

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

[5] Asnicar, F.; Manara, S.; Zolfo, M.; Truong, D. T.; Scholz, M.; Armanini, F.; Ferretti, P.; Gorfer, V.; Pedrotti, A.; Tett, A.; Segata, N. Studying Vertical Microbiome Transmission from Mothers to Infants by Strain-Level Metagenomic Profiling, mSystems, Volume 2 (2017) no. 1 | DOI

[6] Banks, J. A.; Birky, C. W. Chloroplast DNA diversity is low in a wild plant, Lupinus texensis., Proceedings of the National Academy of Sciences, Volume 82 (1985) no. 20, pp. 6950-6954 | DOI

[7] Birky CW, F. P. M. T. Organelle gene diversity under migration, mutation, and drift: Equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes, Genetics, Volume 121 (1898)

[8] 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

[9] 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

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

[11] 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

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

[13] Bary, A. d. Die Erscheinung der Symbiose, De Gruyter, 1879 | DOI

[14] Delignette-Muller, M. L.; Dutang, C. fitdistrplus: AnRPackage for Fitting Distributions, Journal of Statistical Software, Volume 64 (2015) no. 4 | DOI

[15] Douglas, A. E. Symbiotic interactions., Oxford University Press, Oxon, GB, 1994

[16] Douglas, A. E. Conflict, cheats and the persistence of symbioses, New Phytologist, Volume 177 (2008) no. 4, pp. 849-858 | DOI

[17] Douglas, A. E. The Molecular Basis of Bacterial–Insect Symbiosis, Journal of Molecular Biology, Volume 426 (2014) no. 23, pp. 3830-3837 | DOI

[18] Douglas, A. E.; Bouvaine, S.; Russell, R. R. How the insect immune system interacts with an obligate symbiotic bacterium, Proceedings of the Royal Society B: Biological Sciences, Volume 278 (2011) no. 1704, pp. 333-338 | DOI

[19] 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

[20] 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

[21] Funk, D. J.; Wernegreen, J. J.; Moran, N. A. Intraspecific Variation in Symbiont Genomes: Bottlenecks and the Aphid-Buchnera Association, Genetics, Volume 157 (2001) no. 2, pp. 477-489 | DOI

[22] Funkhouser-Jones, L. J.; van Opstal, E. J.; Sharma, A.; Bordenstein, S. R. The Maternal Effect Gene Wds Controls Wolbachia Titer in Nasonia, Current Biology, Volume 28 (2018) no. 11 | DOI

[23] Slothouber Galbreath, J. G. M.; Smith, J. E.; Becnel, J. J.; Butlin, R. K.; Dunn, A. M. Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites?, Biological Invasions, Volume 12 (2009) no. 1, pp. 191-209 | DOI

[24] Hellemans, J.; Mortier, G.; De Paepe, A.; Speleman, F.; Vandesompele, J. Genome Biology, 8 (2007) no. 2 | DOI

[25] Hosokawa, T.; Kikuchi, Y.; Nikoh, N.; Shimada, M.; Fukatsu, T. Strict Host-Symbiont Cospeciation and Reductive Genome Evolution in Insect Gut Bacteria, PLoS Biology, Volume 4 (2006) no. 10 | DOI

[26] HOSOKAWA, T.; KIKUCHI, Y.; FUKATSU, T. How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect-bacterium mutualism?, Molecular Ecology, Volume 16 (2007) no. 24, pp. 5316-5325 | DOI

[27] Ijichi, N.; Kondo, N.; Matsumoto, R.; Shimada, M.; Ishikawa, H.; Fukatsu, T. Internal Spatiotemporal Population Dynamics of Infection with Three Wolbachia Strains in the Adzuki Bean Beetle, Callosobruchus chinensis (Coleoptera: Bruchidae), Applied and Environmental Microbiology, Volume 68 (2002) no. 8, pp. 4074-4080 | DOI

[28] Ikeda, T.; Ishikawa, H.; Sasaki, T. Regulation of Wolbachia Density in the Mediterranean Flour Moth, Ephestia kuehniella, and the Almond Moth, Cadra cautella, Zoological Science, Volume 20 (2003) no. 2, pp. 153-157 | DOI

[29] Kaltenpoth, M.; Goettler, W.; Koehler, S.; Strohm, E. Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission, Evolutionary Ecology, Volume 24 (2010) no. 2, pp. 463-477 | DOI

[30] Kiers, E. T.; Rousseau, R. A.; West, S. A.; Denison, R. F. Host sanctions and the legume–rhizobium mutualism, Nature, Volume 425 (2003) no. 6953, pp. 78-81 | DOI

[31] Lemaitre, B.; Hoffmann, J. The Host Defense of Drosophila melanogaster, Annual Review of Immunology, Volume 25 (2007) no. 1, pp. 697-743 | DOI

[32] Le Pape, S. EasyqpcR : EasyqpcR for easy analysis of real-time PCR data at IRTOMIT-INSERM U1082, 2012 | DOI

[33] Lindsey, A. R. I. Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia, Genes, Volume 11 (2020) no. 7 | DOI

[34] Login, F. H.; Balmand, S.; Vallier, A.; Vincent-Monégat, C.; Vigneron, A.; Weiss-Gayet, M.; Rochat, D.; Heddi, A. Antimicrobial Peptides Keep Insect Endosymbionts Under Control, Science, Volume 334 (2011) no. 6054, pp. 362-365 | DOI

[35] López-Madrigal, S.; Duarte, E. H. Titer regulation in arthropod-Wolbachia symbioses, FEMS Microbiology Letters, Volume 366 (2019) no. 23 | DOI

[36] Mathé‐Hubert, H.; Kaech, H.; Hertaeg, C.; Jaenike, J.; Vorburger, C. Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection, Molecular Ecology, Volume 28 (2019) no. 24, pp. 5330-5346 | DOI

[37] 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

[38] 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

[39] Monnin, D.; Kremer, N.; Michaud, C.; Villa, M.; Henri, H.; Desouhant, E.; Vavre, F. Experimental evolution of virulence and associated traits in a Drosophila melanogaster – Wolbachia symbiosis, bioRxiv (2020) (2020.04.26.062265v4. Peer-reviewed and recommended by PCI Evol Biol) | DOI

[40] Mouton, L.; Henri, H.; Bouletreau, M.; Vavre, F. Strain‐specific regulation of intracellularWolbachiadensity in multiply infected insects, Molecular Ecology, Volume 12 (2003) no. 12, pp. 3459-3465 | DOI

[41] Mouton, L.; Dedeine, F.; Henri, H.; Boulétreau, M.; Profizi, N.; Vavre, F. Virulence, Multiple Infections and Regulation of Symbiotic Population in the Wolbachia-Asobara tabida Symbiosis, Genetics, Volume 168 (2004) no. 1, pp. 181-189 | DOI

[42] Mouton, L.; Henri, H.; Charif, D.; Boulétreau, M.; Vavre, F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis, Biology Letters, Volume 3 (2007) no. 2, pp. 210-213 | DOI

[43] O’Neill, S. L.; Hoffmann, A.; Werren, J. Influential passengers: inherited microorganisms and arthropod reproduction, Oxford University Press., 1997

[44] Parker, B. J.; Hrček, J.; McLean, A. H. C.; Brisson, J. A.; Godfray, H. C. J. Intraspecific variation in symbiont density in an insect–microbe symbiosis, Molecular Ecology, Volume 30 (2021) no. 6, pp. 1559-1569 | DOI

[45] Parkinson, J. F.; Gobin, B.; Hughes, W. O. H. Heritability of symbiont density reveals distinct regulatory mechanisms in a tripartite symbiosis, Ecology and Evolution, Volume 6 (2016) no. 7, pp. 2053-2060 | DOI

[46] Poinsot, D.; Bourtzis, K.; Markakis, G.; Savakis, C.; Merçot, H. Wolbachia Transfer from Drosophila melanogaster into D. simulans: Host Effect and Cytoplasmic Incompatibility Relationships, Genetics, Volume 150 (1998) no. 1, pp. 227-237 | DOI

[47] Rio, R. V.; Wu, Y.-n.; Filardo, G.; Aksoy, S. Dynamics of multiple symbiont density regulation during host development: tsetse fly and its microbial flora, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1588, pp. 805-814 | DOI

[48] Rohrscheib, C. E.; Frentiu, F. D.; Horn, E.; Ritchie, F. K.; van Swinderen, B.; Weible, M. W.; O’Neill, S. L.; Brownlie, J. C. Intensity of Mutualism Breakdown Is Determined by Temperature Not Amplification of Wolbachia Genes, PLOS Pathogens, Volume 12 (2016) no. 9 | DOI

[49] 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

[50] Szathmáry, E.; Smith, J. M. The major evolutionary transitions, Nature, Volume 374 (1995) no. 6519, pp. 227-232 | DOI

[51] Tiivel, T. Cell Symbiosis, Adaptation, and Evolution: Insect-Bacteria Examples In: Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (1991), pp. 170-178

[52] Tipton, L.; Darcy, J. L.; Hynson, N. A. A Developing Symbiosis: Enabling Cross-Talk Between Ecologists and Microbiome Scientists, Frontiers in Microbiology, Volume 10 (2019) | DOI

[53] Vallet-Gely, I.; Lemaitre, B.; Boccard, F. Bacterial strategies to overcome insect defences, Nature Reviews Microbiology, Volume 6 (2008) no. 4, pp. 302-313 | DOI

[54] Veneti, Z.; Clark, M. E.; Karr, T. L.; Savakis, C.; Bourtzis, K. Heads or Tails: Host-Parasite Interactions in the Drosophila-Wolbachia System, Applied and Environmental Microbiology, Volume 70 (2004) no. 9, pp. 5366-5372 | DOI

[55] Vieira, C.; Lepetit, D.; Dumont, S.; Biemont, C. Wake up of transposable elements following Drosophila simulans worldwide colonization, Molecular Biology and Evolution, Volume 16 (1999) no. 9, pp. 1251-1255 | DOI

[56] Vigneron, A.; Masson, F.; Vallier, A.; Balmand, S.; Rey, M.; Vincent-Monégat, C.; Aksoy, E.; Aubailly-Giraud, E.; Zaidman-Rémy, A.; Heddi, A. Insects Recycle Endosymbionts when the Benefit Is Over, Current Biology, Volume 24 (2014) no. 19, pp. 2267-2273 | DOI

[57] Werren, J. H.; Baldo, L.; Clark, M. E. Wolbachia: master manipulators of invertebrate biology, Nature Reviews Microbiology, Volume 6 (2008) no. 10, pp. 741-751 | DOI

[58] Whittaker, J. C.; Harbord, R. M.; Boxall, N.; Mackay, I.; Dawson, G.; Sibly, R. M. Likelihood-Based Estimation of Microsatellite Mutation Rates, Genetics, Volume 164 (2003) no. 2, pp. 781-787 | DOI

[59] You, H.; Lee, W. J.; Lee, W.-J. Homeostasis between gut-associated microorganisms and the immune system in Drosophila, Current Opinion in Immunology, Volume 30 (2014), pp. 48-53 | DOI

[60] Zug, R.; Hammerstein, P. Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia–host interactions, Frontiers in Microbiology, Volume 6 (2015) | DOI

Cited by Sources: