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Summary: Male killing is caused by diverse microbial taxa in a wide range of arthropods . This phenomenon poses important challenges to understanding the dynamics of sex ratios and host-pathogen interactions. However, the mechanisms of male killing are largely unknown. Evidence from one case in Drosophila suggests that bacteria can target components of the male-specific sex-determination pathway . Here, we investigated male killing by the bacterium Arsenophonus nasoniae in the haplo-diploid wasp Nasonia vitripennis, in which females develop as diploids from fertilized eggs and males develop parthenogenetically as haploids from unfertilized eggs. We found that Arsenophonus inhibits the formation of maternal centrosomes, organelles required specifically for early male embryonic development , resulting in unorganized mitotic spindles and developmental arrest well before the establishment of somatic sexual identity. Consistent with these results, rescue of Arsenophonus-induced male lethality was achieved by fertilization with sperm bearing the supernumerary chromosome paternal sex ratio (PSR) , which destroys the paternal genome but bypasses the need for maternal centrosomes by allowing transmission of the sperm-derived centrosome into the egg. These findings reveal a novel mechanism of male killing in Nasonia, demonstrating that bacteria have evolved different mechanisms for inducing male killing in the Arthropods. [Copyright &y& Elsevier]

Summary: A longstanding enigma has been the origin of maternal centrosomes that facilitate parthenogenetic development in Hymenopteran insects. In young embryos, hundreds of microtubule-organizing centers (MTOCs) are assembled completely from maternal components . Two of these MTOCs join the female pronucleus to set up the first mitotic spindle in unfertilized embryos and drive their development . These MTOCs appear to be canonical centrosomes because they contain γ-tubulin, CP190, and centrioles and they undergo duplication . Here, we present evidence that these centrosomes originate from accessory nuclei (AN), organelles derived from the oocyte nuclear envelope . In the parasitic wasps Nasonia vitripennis and Muscidifurax uniraptor, the position and number of AN in mature oocytes correspond to the position and number of maternal centrosomes in early embryos. These AN also contain high concentrations of γ-tubulin. In the honeybee, Apis mellifera, distinct γ-tubulin foci are present in each AN. Additionally, the Hymenopteran homolog of the Drosophila centrosomal protein Dgrip84 localizes on the outer surfaces of AN. These organelles disintegrate in the late oocyte, leaving behind small γ-tubulin foci, which likely seed the formation of maternal centrosomes. Accessory nuclei, therefore, may have played a significant role in the evolution of haplodiploidy in Hymenopteran insects. [Copyright &y& Elsevier]

Summary Numerous arthropods harbor maternally transmitted bacteria that induce the preferential death of males [ 1–7 ]. This sex-specific lethality benefits the bacteria because males are “dead ends” regarding bacterial transmission, and their absence may result in additional resources for their viable female siblings who can thereby more successfully transmit the bacteria [ 5 ]. Although these symbionts disrupt a range of developmental processes [ 8–10 ], the underlying cellular mechanisms are largely unknown. It was previously shown that mutations in genes of the dosage compensation pathway of Drosophila melanogaster suppressed male killing caused by the bacterium, Spiroplasma [ 10 ]. This result suggested that dosage compensation is a target of Spiroplasma . However, it remains unclear how this pathway is affected, and whether the underlying interactions require the male-specific cellular environment. Here, we investigated the cellular basis of male embryonic lethality in D. melanogaster induced by Spiroplasma . We found that the dosage compensation complex (DCC), which acetylates X chromatin in males [ 11 ], becomes mis-localized to ectopic regions of the nucleus immediately prior to the killing phase. This effect was accompanied by inappropriate histone acetylation and genome-wide mis-regulation of gene expression. Artificially induced formation of the DCC in infected females, through transgenic expression of the DCC-specific gene msl-2 , resulted in mis-localization of this complex to non-X regions and early Spiroplasma -induced death, mirroring the killing effects in males. These findings strongly suggest that Spiroplasma initiates male killing by targeting the dosage compensation machinery directly and independently of other cellular features characteristic of the male sex. [ABSTRACT FROM AUTHOR]