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

Alexis Bénard, View ORCID ProfileHélène Henri, Camille Noûs, View ORCID ProfileFabrice Vavre, View ORCID ProfileNatacha Kremer
doi: https://doi.org/10.1101/2020.11.29.402545
Alexis Bénard
1Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
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  • For correspondence: natacha.kremer@normalesup.org alexis.benard@outlook.com
Hélène Henri
1Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
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  • ORCID record for Hélène Henri
Camille Noûs
1Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
2Laboratoire Cogitamus, France
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Fabrice Vavre
1Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
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Natacha Kremer
1Université de Lyon, Université Lyon 1, CNRS, VetAgroSup, Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, Villeurbanne, France
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  • For correspondence: natacha.kremer@normalesup.org alexis.benard@outlook.com
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Abstract

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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Cite as: Bénard A, Henri H, Noûs C, Vavre F, Kremer N (2021) Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors. bioRxiv, 2020.11.29.402545, ver. 4 recommended and peer-reviewed by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.11.29.402545

  • Version 4 of this preprint has been peer-reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100126)

  • https://doi.org/10.5281/zenodo.4607210

  • https://doi.org/10.5281/zenodo.4607223

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 10, 2021.
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Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors
Alexis Bénard, Hélène Henri, Camille Noûs, Fabrice Vavre, Natacha Kremer
bioRxiv 2020.11.29.402545; doi: https://doi.org/10.1101/2020.11.29.402545
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Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors
Alexis Bénard, Hélène Henri, Camille Noûs, Fabrice Vavre, Natacha Kremer
bioRxiv 2020.11.29.402545; doi: https://doi.org/10.1101/2020.11.29.402545

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