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 MK Wolbachia at a low frequency (around 4%) in natural populations of Drosophila pseudotakahashii. MK Wolbachia had a stable density and maternal transmission during laboratory culture, but the MK phenotype which manifested mainly at the larval stage was lost rapidly. MK Wolbachia occurred alongside a second Wolbachia strain expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). A genomic analysis highlighted Wolbachia regions diverged between the 2 strains involving 17 genes, and homologs of the wmk and cif genes implicated in MK and CI were identified in the Wolbachia assembly. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causing Wolbachia. 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.

Cell-based assays and comparative genomics revealed the conserved and hidden effects ofWolbachiaon insect sex determination

“…Under the condition of a female-biased sex ratio, mutations in the host genome that rescue males can be favored by selection. Indeed, the spread of suppressors of symbiont-induced MK has been observed in nature (18,31,(37)(38)(39)(40). For example, the spread of an MK suppressor in the butterfly Hypolimnas bolina was almost complete within 5 years (31,36).…”

“…MK and FM can significantly distort the sex ratio of the host population toward females (13,31,(34)(35)(36). Under extremely female-biased sex ratios, male production is strongly selected, and the development of host resistance to endosymbiont-induced MK has been observed in some insects, such as butterflies, ladybugs, lacewings, and planthoppers (36)(37)(38)(39)(40). However, the subsequent transfer of the 'suppressed' male killer into the genetic background of a new host resulted in the reemergence of MK (30).…”

Ecological drift during colonization drives within- and between-host heterogeneity in animal symbiont populations

“…First, ecological drift can override selection and maintain strain variation within a host population, by providing refugia for suboptimal or less competitive symbionts. In addition, by driving compositional variation between host-associated microbiomes, ecological drift can expose taxonomically or functionally distinctive strains and communities to selection [53,[78][79][80][81][82]. If a distinctive microbiome can maintain its association with a particular host lineage, coevolution with the host may eventually occur.…”

Infection dynamics of endosymbionts that manipulate arthropod reproduction

“…Host defences may impact the efficiency of any reproductive manipulation β, and maternal effects can strongly influence the strength of CI (Wybouw et al, 2022). If hosts evolve traits that limit or even suppress the reproductive manipulation, the spread of resistant hosts hinders the persistence of the endosymbiont (Charlat et al, 2007;Hayashi et al, 2018;Koehncke et al, 2009;Majerus & Majerus, 2010;Richardson et al, 2023). Interestingly, as host suppression of one type of manipulation evolves, some endosymbionts have been shown to switch to another form of manipulation (Hornett et al, 2008).…”