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Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor

Kelly M. Richardson, Perran A. Ross, Brandon S. Cooper, William R. Conner, Tom Schmidt, View ORCID ProfileAry A. Hoffmann
doi: https://doi.org/10.1101/2022.10.19.512817
Kelly M. Richardson
1School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia
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Perran A. Ross
1School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia
2Department of Chemistry and Bioscience, Aalborg University, Aalborg 9220, Denmark
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Brandon S. Cooper
3Division of Biological Sciences, University of Montana, Missoula, MT 59812, US
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William R. Conner
3Division of Biological Sciences, University of Montana, Missoula, MT 59812, US
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Tom Schmidt
1School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia
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Ary A. Hoffmann
1School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia
2Department of Chemistry and Bioscience, Aalborg University, Aalborg 9220, Denmark
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  • ORCID record for Ary A. Hoffmann
  • For correspondence: ary@unimelb.edu.au
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Abstract

Maternally transmitted endosymbiotic bacteria that cause male killing (MK) have only been described from a few insects, but this may reflect challenges in their detection rather than a rarity of MK. Here we identify MK Wolbachia in populations of Drosophila pseudotakahashii, present at a low frequency (around 4%) in natural populations and previously undetected due to a different fixed Wolbachia strain in this species expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). The MK phenotype was eliminated after tetracycline treatment that removed Wolbachia. Molecular analyses indicated the MK phenotype to be expressed when a second Wolbachia strain was present alongside the CI Wolbachia. A genomic analysis highlighted Wolbachia regions diverged between the strains involving 17 genes and also identified the Wolbachia as representing an outgroup to a clade of Wolbachia infecting melanogaster-group species, including wRi-like and wMel-like strains. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causing Wolbachia. The MK phenotype manifested at the larval stage and was transmitted maternally at a high fidelity but with occasional loss of the MK Wolbachia strain. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of the D. pseudotakahashii genome. These findings highlight the complexity of nuclear and microbial components affecting MK endosymbiont detection and dynamics in populations, and the challenges of making connections between endosymbionts and the host phenotypes affected by them.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted October 22, 2022.
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Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor
Kelly M. Richardson, Perran A. Ross, Brandon S. Cooper, William R. Conner, Tom Schmidt, Ary A. Hoffmann
bioRxiv 2022.10.19.512817; doi: https://doi.org/10.1101/2022.10.19.512817
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Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor
Kelly M. Richardson, Perran A. Ross, Brandon S. Cooper, William R. Conner, Tom Schmidt, Ary A. Hoffmann
bioRxiv 2022.10.19.512817; doi: https://doi.org/10.1101/2022.10.19.512817

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