The phage gene wmk is a candidate for male killing by a bacterial endosymbiont.

Jessamyn I Perlmutter,Jason A Metcalf,Seth R Bordenstein,Francis M Jiggins,Julien Martinez,Tom Hill,Robert L Unckless,Sarah R Bordenstein,Daniel P Lepage,David S Schneider

doi:10.1371/journal.ppat.1007936

Abstract

Wolbachia are the most widespread maternally-transmitted bacteria in the animal kingdom. Their global spread in arthropods and varied impacts on animal physiology, evolution, and vector control are in part due to parasitic drive systems that enhance the fitness of infected females, the transmitting sex of Wolbachia. Male killing is one common drive mechanism wherein the sons of infected females are selectively killed. Despite decades of research, the gene(s) underlying Wolbachia-induced male killing remain unknown. Here using comparative genomic, transgenic, and cytological approaches in fruit flies, we identify a candidate gene in the eukaryotic association module of Wolbachia prophage WO, termed WO-mediated killing (wmk), which transgenically causes male-specific lethality during early embryogenesis and cytological defects typical of the pathology of male killing. The discovery of wmk establishes new hypotheses for the potential role of phage genes in sex-specific lethality, including the control of arthropod pests and vectors.

Highlights

Wolbachia infect an estimated 40–52% of all arthropod species [1, 2] and 47% of filarial nematode species [3], making them the most widespread intracellular bacterial symbiont in animals
Male killing is an adaptive trait for bacteria that are maternally transmitted through host populations
We demonstrate that a single gene from the eukaryotic association module in prophage WO of Wolbachia is a candidate for male killing as it recapitulates many aspects of the phenotype when transgenically expressed in fruit flies

Summary

Introduction

Wolbachia (order Rickettsiales) infect an estimated 40–52% of all arthropod species [1, 2] and 47% of filarial nematode species [3], making them the most widespread intracellular bacterial symbiont in animals. In arthropod reproductive tissues and embryos, Wolbachia deploy cunning manipulations to achieve a greater proportion of transmitting females in the host population. These strategies are categorized as reproductive parasitism. Selective death of an infected female’s sons [6], is one such form of reproductive parasitism [7, 8] It enhances the fitness of Wolbachia-infected females in three potential ways: (i) reducing brother-sister competition for limited resources [9], (ii) reducing inbreeding [10], and/or (iii) providing nutrients in cases where infected sisters cannibalize embryos of their dead brothers [10]. Male-killing Spiroplasma [13], Rickettsia [10], and Arsenophonus [14] occur in diverse hosts including flies [13], ladybugs [10], and wasps [14]

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