A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

Abstract

Bacteria that live inside the cells of insect hosts (endosymbionts) can alter the reproduction of their hosts, including the killing of male offspring (male killing, MK). MK has only been described in a few insects, but this may reflect challenges in detecting MK rather than its rarity. Here, we identify MKWolbachiaat a low frequency (around 4%) in natural populations ofDrosophila pseudotakahashii. MKWolbachiahad a stable density and maternal transmission during laboratory culture, but the MK phenotype which manifested mainly at the larval stage was lost rapidly. MKWolbachiaoccurred alongside a secondWolbachiastrain expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). A genomic analysis highlightedWolbachiaregions diverged between the 2 strains involving 17 genes, and homologs of thewmkandcifgenes implicated in MK and CI were identified in theWolbachiaassembly. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causingWolbachia. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of theD.pseudotakahashiigenome. 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.