Prophage-encodedHm-oscargene recapitulatesWolbachia-induced male killing in the tea tortrix mothHomona magnanima

Abstract

Wolbachiaare the maternally transmitted bacterial symbionts that are ubiquitous among arthropods. They can hijack host reproduction in various ways, including male killing (MK), where the sons of infected mothers are killed during development. The recent discovery of MK-associatedWolbachiagenes, i.e.,oscarinOstriniamoths andwmkinDrosophilaflies, stimulates our interest in the diversity and commonality of MK mechanisms, which remain largely unclear. We recently discovered that aWolbachiasymbiont of the mothHomona magnanimacarries an MK-associated prophage region encoding homologs ofoscar(Hm-oscar) andwmk(wmk-1–4). Here, we investigated the effects of these genes in the native host. Upon transient overexpression,Hm-oscar, but notwmk, induced male lethality inH. magnanima, in contrast to our observations inDrosophila, where thewmkhomologs, but notHm-oscar, killed the males.Hm-oscardisrupted sex determination in male embryos by inducing a female-typedoublesexsplicing and impaired dosage compensation, recapitulating theWolbachiaphenotype. Cell-based transfection assays confirmed thatHm-oscarsuppressed the function ofmasculinizer, the upstream male sex determinant involved in lepidopteran dosage compensation. Our study highlights the conserved roles ofoscarhomologs inWolbachia-induced lepidopteran MK and argues thatWolbachiahave evolved multiple MK mechanisms in insects.