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Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis.

ABSTRACT: Wolbachia are the most abundant maternally inherited endosymbionts of insects and cause various reproductive alterations in their hosts. One such manipulation is cytoplasmic incompatibility (CI), which is a sperm-egg incompatibility typically resulting in zygotic death. Nasonia longicornis (Hymenoptera: Pteromalidae) has an A supergroup and two closely related B supergroup Wolbachia infections. The B supergroup bacteria co-diverged in this host genus. Both triple (wNlonAwNlonB1wNlonB2) and double infections (wNlonAwNlonB1, wNlonAwNlonB2) have been obtained from the field. In the present study, CI was determined among the three Wolbachia types in different host genetic backgrounds. Results show that host genetic background determines whether bidirectional CI or unidirectional CI occurs between the two closely related B group Wolbachia. Results show that the wNlonB1-infected males are bidirectionally incompatible with wNlonB2 in their 'native' nuclear genetic background, whereas wNlonB1 males are compatible with wNlonB2 in two other N. longicornis genetic backgrounds, resulting in unidirectional CI. In contrast, wNlonB2-infected males are incompatible with wNlonB1 females in all three host genetic backgrounds. These changes in incompatibility are not due to the loss of the bacteria. We hypothesize that a repressor gene for sperm modification by wNlonB1 is segregating in N. longicornis populations. The relevance of these findings to the potential role of Wolbachia in host-reproductive divergence and speciation is discussed.

SUBMITTER: Raychoudhury R

PROVIDER: S-EPMC3262870 | biostudies-other | 2012 Feb

REPOSITORIES: biostudies-other

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Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis.

Raychoudhury R R Werren J H JH

Heredity 20110727 2

Wolbachia are the most abundant maternally inherited endosymbionts of insects and cause various reproductive alterations in their hosts. One such manipulation is cytoplasmic incompatibility (CI), which is a sperm-egg incompatibility typically resulting in zygotic death. Nasonia longicornis (Hymenoptera: Pteromalidae) has an A supergroup and two closely related B supergroup Wolbachia infections. The B supergroup bacteria co-diverged in this host genus. Both triple (wNlonAwNlonB1wNlonB2) and doubl ...[more]

PMID: 21792226

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Project description:BackgroundBacteria of the genus Wolbachia are reproductive parasites widespread among arthropods. The most common effect arising from the presence of Wolbachia in a population is Cytoplasmic Incompatibility (CI), whereby postmating reproductive isolation occurs in crosses between an infected male and an uninfected female, or when a male is infected with a different strain of Wolbachia to that of the female (bidirectional CI). Previous theoretical models have demonstrated that bidirectional CI can contribute to the genetic divergence of populations in haploid and diploid organisms. However, haplodiploid organisms were not considered in these models even though they include Nasonia parasitoid wasps - the best example of the implication of Wolbachia in ongoing speciation. Moreover, previous work did not investigate inbreeding mating systems, which are frequently observed in arthropod species.ResultsWe developed a stochastic two-island model which simulated three genetic scenarios, diploidy, haploidy, and haplodiploidy, with two CI phenotypes being considered for the latter: (1) male development of female progeny; and (2) mortality of fertilized eggs. We also investigated the effect of varying the proportion of sib mating. In the model each allopatric population was initially fixed for a single allele at a nuclear locus under positive selection and infected with one strain of Wolbachia. Each simulation presupposed that the two populations were fixed for a different allele and a different strain of Wolbachia. The degree of genetic differentiation observed in the locus under selection due to bidirectional CI was much lower for the two haplodiploid phenotypes than for either diploids or haploids. Furthermore, we demonstrated that sib-mating may compensate for the lower efficiency of bidirectional CI in haplodiploids by maintaining genetic divergence.ConclusionOur model suggests that maintenance of genetic differentiation facilitated by Wolbachia is more likely to occur in diploids and haploids than in haplodiploids. However, increasing the level of sib-mating may compensate for the weak effect of bidirectional CI in haplodiploids. Our work therefore gives a potential explanation for why the haplodiploid Nasonia species, which are infected with bidirectionally incompatible Wolbachia strains and undergo sib-mating, have differentiated genetically and maintained this differentiation without premating isolation.

Project description:Cytoplasmic incompatibility (CI) is an intriguing, widespread, symbiont-induced reproductive failure that decreases offspring production of arthropods through crossing incompatibility of infected males with uninfected females or with females infected with a distinct symbiont genotype. For years, the molecular mechanism of CI remained unknown. Recent genomic, proteomic, biochemical, and cell biological studies have contributed to understanding of CI in the alphaproteobacterium Wolbachia and implicate genes associated with the WO prophage. Besides a recently discovered additional lineage of alphaproteobacterial symbionts only moderately related to Wolbachia, Cardinium (Bacteroidetes) is the only other symbiont known to cause CI, and genomic evidence suggests that it has very little homology with Wolbachia and evolved this phenotype independently. Here, we present the first transcriptomic study of the CI Cardinium strain cEper1, in its natural host, Encarsia suzannae, to detect important CI candidates and genes involved in the insect-Cardinium symbiosis. Highly expressed transcripts included genes involved in manipulating ubiquitination, apoptosis, and host DNA. Female-biased genes encoding ribosomal proteins suggest an increase in general translational activity of Cardinium in female wasps. The results confirm previous genomic analyses that indicated that Wolbachia and Cardinium utilize different genes to induce CI, and transcriptome patterns further highlight expression of some common pathways that these bacteria use to interact with the host and potentially cause this enigmatic and fundamental manipulation of host reproduction. IMPORTANCE The majority of insects carry maternally inherited intracellular bacteria that are important in their hosts' biology, ecology, and evolution. Some of these bacterial symbionts cause a reproductive failure known as cytoplasmic incompatibility (CI). In CI, the mating of symbiont-infected males and uninfected females produces few or no daughters. The CI symbiont then spreads and can have a significant impact on the insect host population. Cardinium, a bacterial endosymbiont of the parasitoid wasp Encarsia in the Bacteroidetes, is the only bacterial lineage known to cause CI outside the Alphaproteobacteria, where Wolbachia and another recently discovered CI symbiont reside. Here, we sought insight into the gene expression of a CI-inducing Cardinium strain in its natural host, Encarsia suzannae. Our study provides the first insights into the Cardinium transcriptome and provides support for the hypothesis that Wolbachia and Cardinium target similar host pathways with distinct and largely unrelated sets of genes.

Project description:BackgroundThe endosymbiont Wolbachia can manipulate arthropod reproduction and invade host populations by inducing cytoplasmic incompatibility (CI). Some host species are coinfected with multiple Wolbachia strains which may have sequentially invaded host populations by expressing different types of modular CI factor (cif) genes. The tephritid fruit fly Rhagoletis cerasi is a model for CI and Wolbachia population dynamics. It is associated with at least four Wolbachia strains in various combinations, with demonstrated (wCer2, wCer4), predicted (wCer1) or unknown (wCer5) CI phenotypes.ResultsWe sequenced and assembled the draft genomes of the Wolbachia strains wCer1, wCer4 and wCer5, and compared these with the previously sequenced genome of wCer2 which currently invades R. cerasi populations. We found complete cif gene pairs in all strains: four pairs in wCer2 (three Type I; one Type V), two pairs in wCer1 (both Type I) and wCer4 (one Type I; one Type V), and one pair in wCer5 (Type IV). Wolbachia genome variant analyses across geographically and genetically distant host populations revealed the largest diversity of single nucleotide polymorphisms (SNPs) in wCer5, followed by wCer1 and then wCer2, indicative of their different lengths of host associations. Furthermore, mitogenome analyses of the Wolbachia genome-sequenced individuals in combination with SNP data from six European countries revealed polymorphic mitogenome sites that displayed reduced diversity in individuals infected with wCer2 compared to those without.ConclusionsCoinfections with Wolbachia are common in arthropods and affect options for Wolbachia-based management strategies of pest and vector species already infected by Wolbachia. Our analyses of Wolbachia genomes of a host naturally coinfected by several strains unravelled signatures of the evolutionary dynamics in both Wolbachia and host mitochondrial genomes as a consequence of repeated invasions. Invasion of already infected populations by new Wolbachia strains requires new sets of functionally different cif genes and thereby may select for a cumulative modularity of cif gene diversity in invading strains. Furthermore, we demonstrated at the mitogenomic scale that repeated CI-driven Wolbachia invasions of hosts result in reduced mitochondrial diversity and hitchhiking effects. Already resident Wolbachia strains may experience similar cytoplasmic hitchhiking effects caused by the invading Wolbachia strain.

Dataset Information

Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis.

Publications

Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis.

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