High Incidence of Related Wolbachia across Unrelated Leaf-Mining Diptera

The maternally inherited endosymbiont, Wolbachia pipientis, plays an important role in the ecology and evolution of many of its hosts by affecting host reproduction and fitness. Here, we investigated 13 dipteran leaf-mining species to characterize Wolbachia infections and the potential for this endosymbiont in biocontrol. Wolbachia infections were present in 12 species, including 10 species where the Wolbachia infection was at or near fixation. A comparison of Wolbachia relatedness based on the wsp/MLST gene set showed that unrelated leaf-mining species often shared similar Wolbachia, suggesting common horizontal transfer. We established a colony of Liriomyza brassicae and found adult Wolbachia density was stable; although Wolbachia density differed between the sexes, with females having a 20-fold higher density than males. Wolbachia density increased during L. brassicae development, with higher densities in pupae than larvae. We removed Wolbachia using tetracycline and performed reciprocal crosses between Wolbachia-infected and uninfected individuals. Cured females crossed with infected males failed to produce offspring, indicating that Wolbachia induced complete cytoplasmic incompatibility in L. brassicae. The results highlight the potential of Wolbachia to suppress Liriomyza pests based on approaches such as the incompatible insect technique, where infected males are released into populations lacking Wolbachia or with a different incompatible infection.

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Wolbachia infection reduces sperm competitive ability in an insect

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2006.3478 ◽

2006 ◽

Vol 273 (1593) ◽

pp. 1455-1458 ◽

Cited By ~ 69

Author(s):

Fleur E Champion de Crespigny ◽

Nina Wedell

Keyword(s):

Population Dynamics ◽

Sperm Competition ◽

Empirical Evidence ◽

Reproductive Strategies ◽

Competitive Ability ◽

Cytoplasmic Incompatibility ◽

Wolbachia Infection ◽

Sperm Production ◽

Fitness Costs ◽

Wolbachia Pipientis

The maternally inherited bacterium Wolbachia pipientis imposes significant fitness costs on its hosts. One such cost is decreased sperm production resulting in reduced fertility of male Drosophila simulans infected with cytoplasmic incompatibility (CI) inducing Wolbachia . We tested the hypothesis that Wolbachia infection affects sperm competitive ability and found that Wolbachia infection is indeed associated with reduced success in sperm competition in non-virgin males. In the second male role, infected males sired 71% of the offspring whereas uninfected males sired 82% of offspring. This is the first empirical evidence indicating that Wolbachia infection deleteriously affects sperm competition and raises the possibility that polyandrous females can utilize differential sperm competitive ability to bias the paternity of broods and avoid the selfish manipulations of Wolbachia . This suggests a relationship between Wolbachia infection and host reproductive strategies. These findings also have important consequences for Wolbachia population dynamics because the transmission advantage of Wolbachia is likely to be undermined by sperm competition.

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The Detection of Wolbachia in Tea Green Leafhopper (Empoasca onukii Matsuda) and Its Influence on the Host

Agriculture ◽

10.3390/agriculture12010036 ◽

2021 ◽

Vol 12 (1) ◽

pp. 36

Author(s):

Qiuqiu Zhang ◽

Rongmeng Lan ◽

Dezhong Ji ◽

Yanni Tan ◽

Xia Zhou ◽

...

Keyword(s):

Cytoplasmic Incompatibility ◽

Reproductive Factors ◽

Wolbachia Infection ◽

Green Leafhopper ◽

High Incidence ◽

Biased Sex Ratio ◽

Tea Production ◽

Polymerase Chain ◽

Development And Evolution

Tea green leafhopper (Empoasca onukii Matsuda) is a critical pest in tea production. Wolbachia has attracted much attention as a new direction of pest biological control for its ability of manipulating the hosts’ reproductive biology. In this work, we focused on the detection of Wolbachia in tea green leafhopper and its effect on host reproduction and development. Polymerase chain reaction (PCR), real-time PCR, and fluorescence in situ hybridization (FISH) techniques were used to detect the distribution of Wolbachia in tea green leafhopper. Wolbachia infection levels were different in different organs of hosts in different insect stages. In addition, comparison between the infected populations and cured population (treated by tetracyclines) revealed that presence of Wolbachia apparently influenced the growth, life cycle, and other reproductive factors of tea green leafhopper, caused, for example, by cytoplasmic incompatibility (CI), thereby reducing number of offspring, shortening lifespan, and causing female-biased sex ratio. This research confirmed that the bacteria Wolbachia was of high incidence in tea leafhoppers and could significantly affect the hosts’ reproductive development and evolution.

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Wolbachia infection lowers fertile sperm transfer in a moth

Biology Letters ◽

10.1098/rsbl.2010.0605 ◽

2010 ◽

Vol 7 (2) ◽

pp. 187-189 ◽

Cited By ~ 22

Author(s):

Z. Lewis ◽

F. E. Champion de Crespigny ◽

S. M. Sait ◽

T. Tregenza ◽

N. Wedell

Keyword(s):

Cytoplasmic Incompatibility ◽

Wolbachia Infection ◽

Ephestia Kuehniella ◽

Sperm Transfer ◽

Endosymbiotic Bacterium ◽

Sperm Production ◽

Wolbachia Pipientis ◽

Zygote Development ◽

Apyrene Sperm ◽

Mediterranean Flour Moth

The endosymbiotic bacterium Wolbachia pipientis manipulates host reproduction by rendering infected males reproductively incompatible with uninfected females (cytoplasmic incompatibility; CI). CI is believed to occur as a result of Wolbachia -induced modifications to sperm during maturation, which prevent infected sperm from initiating successful zygote development when fertilizing uninfected females' eggs. However, the mechanism by which CI occurs has been little studied outside the genus Drosophila . Here, we show that in the sperm heteromorphic Mediterranean flour moth, Ephestia kuehniella , infected males transfer fewer fertile sperm at mating than uninfected males. In contrast, non-fertile apyrene sperm are not affected. This indicates that Wolbachia may only affect fertile sperm production and highlights the potential of the Lepidoptera as a model for examining the mechanism by which Wolbachia induces CI in insects.

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Wolbachia Density and Cytoplasmic Incompatibility in Aedes albopictus: Concerns with Using Artificial Wolbachia Infection as a Vector Suppression Tool

PLoS ONE ◽

10.1371/journal.pone.0121813 ◽

2015 ◽

Vol 10 (3) ◽

pp. e0121813 ◽

Cited By ~ 36

Author(s):

Maurizio Calvitti ◽

Francesca Marini ◽

Angiola Desiderio ◽

Arianna Puggioli ◽

Riccardo Moretti

Keyword(s):

Aedes Albopictus ◽

Cytoplasmic Incompatibility ◽

Wolbachia Infection ◽

Wolbachia Density

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Wolbachia and Cytoplasmic Incompatibility in the CaliforniaCulex pipiensMosquito Species Complex: Parameter Estimates and Infection Dynamics in Natural Populations

Genetics ◽

10.1093/genetics/165.4.2029 ◽

2003 ◽

Vol 165 (4) ◽

pp. 2029-2038 ◽

Cited By ~ 3

Author(s):

Jason L Rasgon ◽

Thomas W Scott

Keyword(s):

Species Complex ◽

Cytoplasmic Incompatibility ◽

Natural Populations ◽

Wolbachia Infection ◽

Field Conditions ◽

Parameter Estimates ◽

Infection Prevalence ◽

Infection Frequency ◽

Specific Pcr ◽

Vector Borne

AbstractBefore maternally inherited bacterial symbionts like Wolbachia, which cause cytoplasmic incompatibility (CI; reduced hatch rate) when infected males mate with uninfected females, can be used in a program to control vector-borne diseases it is essential to understand their dynamics of infection in natural arthropod vector populations. Our study had four goals: (1) quantify the number of Wolbachia strains circulating in the California Culex pipiens species complex, (2) investigate Wolbachia infection frequencies and distribution in natural California populations, (3) estimate the parameters that govern Wolbachia spread among Cx. pipiens under laboratory and field conditions, and (4) use these values to estimate equilibrium levels and compare predicted infection prevalence levels to those observed in nature. Strain-specific PCR, wsp gene sequencing, and crossing experiments indicated that a single Wolbachia strain infects Californian Cx. pipiens. Infection frequency was near or at fixation in all populations sampled for 2 years along a >1000-km north-south transect. The combined statewide infection frequency was 99.4%. Incompatible crosses were 100% sterile under laboratory and field conditions. Sterility decreased negligibly with male age in the laboratory. Infection had no significant effect on female fecundity under laboratory or field conditions. Vertical transmission was >99% in the laboratory and ∼98.6% in the field. Using field data, models predicted that Wolbachia will spread to fixation if infection exceeds an unstable equilibrium point above 1.4%. Our estimates accurately predicted infection frequencies in natural populations. If certain technical hurdles can be overcome, our data indicate that Wolbachia can invade vector populations as part of an applied transgenic strategy for vector-borne disease reduction.

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Titer regulation in arthropod-Wolbachia symbioses

FEMS Microbiology Letters ◽

10.1093/femsle/fnz232 ◽

2019 ◽

Vol 366 (23) ◽

Cited By ~ 10

Author(s):

Sergio López-Madrigal ◽

Elves H Duarte

Keyword(s):

Wolbachia Infection ◽

Intracellular Bacteria ◽

Biological Factors ◽

Wolbachia Pipientis ◽

Host Fitness ◽

Symbiotic Associations ◽

Infection Dynamics ◽

Wide Range ◽

High Prevalence ◽

Fine Regulation

ABSTRACT Symbiosis between intracellular bacteria (endosymbionts) and animals are widespread. The alphaproteobacterium Wolbachia pipientis is known to maintain a variety of symbiotic associations, ranging from mutualism to parasitism, with a wide range of invertebrates. Wolbachia infection might deeply affect host fitness (e.g. reproductive manipulation and antiviral protection), which is thought to explain its high prevalence in nature. Bacterial loads significantly influence both the infection dynamics and the extent of bacteria-induced host phenotypes. Hence, fine regulation of bacterial titers is considered as a milestone in host-endosymbiont interplay. Here, we review both environmental and biological factors modulating Wolbachia titers in arthropods.

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The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria

Genes ◽

10.3390/genes11080852 ◽

2020 ◽

Vol 11 (8) ◽

pp. 852

Author(s):

Hongli Chen ◽

Mengwen Zhang ◽

Mark Hochstrasser

Keyword(s):

Molecular Mechanisms ◽

Protein Pair ◽

Cytoplasmic Incompatibility ◽

Wolbachia Infection ◽

Threshold Level ◽

Upstream Gene ◽

Arthropod Species ◽

Bacterial Endosymbionts ◽

Inducing Factors ◽

New Research

Many species of arthropods carry maternally inherited bacterial endosymbionts that can influence host sexual reproduction to benefit the bacterium. The most well-known of such reproductive parasites is Wolbachia pipientis. Wolbachia are obligate intracellular α-proteobacteria found in nearly half of all arthropod species. This success has been attributed in part to their ability to manipulate host reproduction to favor infected females. Cytoplasmic incompatibility (CI), a phenomenon wherein Wolbachia infection renders males sterile when they mate with uninfected females, but not infected females (the rescue mating), appears to be the most common. CI provides a reproductive advantage to infected females in the presence of a threshold level of infected males. The molecular mechanisms of CI and other reproductive manipulations, such as male killing, parthenogenesis, and feminization, have remained mysterious for many decades. It had been proposed by Werren more than two decades ago that CI is caused by a Wolbachia-mediated sperm modification and that rescue is achieved by a Wolbachia-encoded rescue factor in the infected egg. In the past few years, new research has highlighted a set of syntenic Wolbachia gene pairs encoding CI-inducing factors (Cifs) as the key players for the induction of CI and its rescue. Within each Cif pair, the protein encoded by the upstream gene is denoted A and the downstream gene B. To date, two types of Cifs have been characterized based on the enzymatic activity identified in the B protein of each protein pair; one type encodes a deubiquitylase (thus named CI-inducing deubiquitylase or cid), and a second type encodes a nuclease (named CI-inducing nuclease or cin). The CidA and CinA proteins bind tightly and specifically to their respective CidB and CinB partners. In transgenic Drosophila melanogaster, the expression of either the Cid or Cin protein pair in the male germline induces CI and the expression of the cognate A protein in females is sufficient for rescue. With the identity of the Wolbachia CI induction and rescue factors now known, research in the field has turned to directed studies on the molecular mechanisms of CI, which we review here.

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Environmental Concentrations of Antibiotics May Diminish Wolbachia infections in Aedes aegypti (Diptera: Culicidae)

Journal of Medical Entomology ◽

10.1093/jme/tjz023 ◽

2019 ◽

Vol 56 (4) ◽

pp. 1078-1086 ◽

Cited By ~ 6

Author(s):

Nancy M Endersby-Harshman ◽

Jason K Axford ◽

Ary A Hoffmann

Keyword(s):

Aedes Aegypti ◽

Cytoplasmic Incompatibility ◽

South East Asia ◽

Tetracycline Antibiotics ◽

Tropical Regions ◽

Breeding Sites ◽

Septic Tanks ◽

Dengue Transmission ◽

Wolbachia Density ◽

Subterranean Water

Abstract Wolbachia-infected Aedes aegypti (L.) mosquitoes for control of dengue transmission are being released experimentally in tropical regions of Australia, south-east Asia, and South America. To become established, the Wolbachia Hertig (Rickettsiales: Rickettsiaceae) strains used must induce expression of cytoplasmic incompatibility (CI) in matings between infected males and uninfected females so that infected females have a reproductive advantage, which will drive the infection through field populations. Wolbachia is a Rickettsia-like alphaproteobacterium which can be affected by tetracycline antibiotics. We investigated whether exposure of Wolbachia-infected mosquitoes to chlortetracycline at environmentally relevant levels during their aquatic development resulted in loss or reduction of infection in three strains, wAlbB, wMel, and wMelPop. Wolbachia density was reduced for all three strains at the tested chlortetracycline concentrations of 5 and 50 µg/liter. Two of the strains, wMel and wMelPop, showed a breakdown in CI. The wAlbB strain maintained CI and may be useful at breeding sites where tetracycline contamination has occurred. This may include drier regions where Ae. aegypti can utilize subterranean water sources and septic tanks as breeding sites.

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Wolbachia Endosymbiont of the Horn Fly (Haematobia irritans irritans): a Supergroup A Strain with Multiple Horizontally Acquired Cytoplasmic Incompatibility Genes

Applied and Environmental Microbiology ◽

10.1128/aem.02589-19 ◽

2020 ◽

Vol 86 (6) ◽

Cited By ~ 6

Author(s):

Mukund Madhav ◽

Rhys Parry ◽

Jess A. T. Morgan ◽

Peter James ◽

Sassan Asgari

Keyword(s):

Cytoplasmic Incompatibility ◽

The United States ◽

Whole Genome ◽

Evolutionary Analysis ◽

Content Type ◽

Wolbachia Pipientis ◽

Haematobia Irritans ◽

Horn Fly ◽

Horn Flies ◽

Horizontal Acquisition

ABSTRACT The horn fly, Haematobia irritans irritans, is a hematophagous parasite of livestock distributed throughout Europe, Africa, Asia, and the Americas. Welfare losses on livestock due to horn fly infestation are estimated to cost between $1 billion and $2.5 billion (U.S. dollars) annually in North America and Brazil. The endosymbiotic bacterium Wolbachia pipientis is a maternally inherited manipulator of reproductive biology in arthropods and naturally infects laboratory colonies of horn flies from Kerrville, TX, and Alberta, Canada, but it has also been identified in wild-caught samples from Canada, the United States, Mexico, and Hungary. Reassembly of PacBio long-read and Illumina genomic DNA libraries from the Kerrville H. i. irritans genome project allowed for a complete and circularized 1.3-Mb Wolbachia genome (wIrr). Annotation of wIrr yielded 1,249 coding genes, 34 tRNAs, 3 rRNAs, and 5 prophage regions. Comparative genomics and whole-genome Bayesian evolutionary analysis of wIrr compared to published Wolbachia genomes suggested that wIrr is most closely related to and diverged from Wolbachia supergroup A strains known to infect Drosophila spp. Whole-genome synteny analyses between wIrr and closely related genomes indicated that wIrr has undergone significant genome rearrangements while maintaining high nucleotide identity. Comparative analysis of the cytoplasmic incompatibility (CI) genes of wIrr suggested two phylogenetically distinct CI loci and acquisition of another cifB homolog from phylogenetically distant supergroup A Wolbachia strains, suggesting horizontal acquisition of these loci. The wIrr genome provides a resource for future examination of the impact Wolbachia may have in both biocontrol and potential insecticide resistance of horn flies. IMPORTANCE Horn flies, Haematobia irritans irritans, are obligate hematophagous parasites of cattle having significant effects on production and animal welfare. Control of horn flies mainly relies on the use of insecticides, but issues with resistance have increased interest in development of alternative means of control. Wolbachia pipientis is an endosymbiont bacterium known to have a range of effects on host reproduction, such as induction of cytoplasmic incompatibility, feminization, male killing, and also impacts vector transmission. These characteristics of Wolbachia have been exploited in biological control approaches for a range of insect pests. Here we report the assembly and annotation of the circular genome of the Wolbachia strain of the Kerrville, TX, horn fly (wIrr). Annotation of wIrr suggests its unique features, including the horizontal acquisition of additional transcriptionally active cytoplasmic incompatibility loci. This study provides the foundation for future studies of Wolbachia-induced biological effects for control of horn flies.

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The Intracellular Symbiont Wolbachia pipientis Enhances Recombination in a Dose-Dependent Manner

Insects ◽

10.3390/insects11050284 ◽

2020 ◽

Vol 11 (5) ◽

pp. 284

Author(s):

Kaeli N. Bryant ◽

Irene L. G. Newton

Keyword(s):

Drosophila Melanogaster ◽

Horizontal Transmission ◽

Wolbachia Infection ◽

Wolbachia Strain ◽

Dependent Manner ◽

Predator Prey ◽

Wolbachia Pipientis ◽

Intracellular Symbiont ◽

Dose Dependent ◽

Classical Genetics

Wolbachia pipientis is an intracellular alphaproteobacterium that infects 40%–60% of insect species and is well known for host reproductive manipulations. Although Wolbachia are primarily maternally transmitted, evidence of horizontal transmission can be found in incongruent host–symbiont phylogenies and recent acquisitions of the same Wolbachia strain by distantly related species. Parasitoids and predator–prey interactions may indeed facilitate the transfer of Wolbachia between insect lineages, but it is likely that Wolbachia are acquired via introgression in many cases. Many hypotheses exist to explain Wolbachia prevalence and penetrance, such as nutritional supplementation, protection from parasites, protection from viruses, or direct reproductive parasitism. Using classical genetics, we show that Wolbachia increase recombination in infected lineages across two genomic intervals. This increase in recombination is titer-dependent as the wMelPop variant, which infects at higher load in Drosophila melanogaster, increases recombination 5% more than the wMel variant. In addition, we also show that Spiroplasma poulsonii, another bacterial intracellular symbiont of D. melanogaster, does not induce an increase in recombination. Our results suggest that Wolbachia infection specifically alters its host’s recombination landscape in a dose-dependent manner.

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