Common and unique strategies of male killing evolved in two distinct<i>Drosophila</i>symbionts

Abstract

Male killing is a selfish reproductive manipulation caused by symbiotic bacteria, where male offspring of infected hosts are selectively killed. The underlying mechanisms and the process of their evolution are of great interest not only in terms of fundamental biology, but also their potential applications. The two bacterial <i>Drosophila</i> symbionts, <i>Wolbachia</i> and <i>Spiroplasma</i>, have independently evolved male-killing ability. This raises the question whether the underlying mechanisms share some similarities or are specific to each bacterial species. Here, we analyse pathogenic phenotypes of <i>D. bifasciata</i> infected with its natural male-killing <i>Wolbachia</i> strain and compare them with those of <i>D. melanogaster</i> infected with male-killing <i>Spiroplasma</i> We show that male progeny infected with the <i>Wolbachia</i> strain die during embryogenesis with abnormal apoptosis. Interestingly, male-killing <i>Wolbachia</i> infection induces DNA damage and segregation defects in the dosage-compensated chromosome in male embryos, which are reminiscent of the phenotypes caused by male-killing <i>Spiroplasma</i> in <i>D. melanogaster</i> By contrast, host neural development seems to proceed normally unlike male-killing <i>Spiroplasma</i> infection. Our results demonstrate that the dosage-compensated chromosome is a common target of two distinct male killers, yet <i>Spiroplasma</i> uniquely evolved the ability to damage neural tissue of male embryos.