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

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 StatementThe authors have declared no competing interest.

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