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Genetics. Nov 2002; 162(3): 1313–1319.
PMCID: PMC1462327

Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella.


Wolbachia is known as the causative agent of various reproductive alterations in arthropods. The almond moth Cadra cautella is doubly infected with A- and B-group Wolbachia and expresses complete cytoplasmic incompatibility (CI). The Mediterranean flour moth Ephestia kuehniella carries A-group Wolbachia and expresses partial CI. In the present study, the Wolbachia in C. cautella was transferred to E. kuehniella from which the original Wolbachia had been removed. We obtained transfected lines of three different infection states: single infection with A, single infection with B, and double infection with A and B. The doubly transfected lines and those transfected with only A produced exclusively female progeny. Two lines of evidence suggested that the sex ratio distortion was due to male killing. First, reduced egg hatch rate was observed. Second, removal of the Wolbachia from the transfected lines resulted in the recovery of a normal sex ratio of approximately 1:1. The occurrence of male killing following transfection showed that host factors influence the determination of the reproductive phenotype caused by Wolbachia. The transfected E. kuehniella males carrying exclusively B-group Wolbachia expressed partial incompatibility when crossed with the uninfected females. In addition, the transfected lines were bidirectionally incompatible with the naturally infected strain, which was the first demonstration of bidirectional CI in a lepidopteran.

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Selected References

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  • Bouchon D, Rigaud T, Juchault P. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci. 1998 Jun 22;265(1401):1081–1090. [PMC free article] [PubMed]
  • Boyle L, O'Neill SL, Robertson HM, Karr TL. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science. 1993 Jun 18;260(5115):1796–1799. [PubMed]
  • Braig HR, Guzman H, Tesh RB, O'Neill SL. Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature. 1994 Feb 3;367(6462):453–455. [PubMed]
  • Breeuwer JA, Werren JH. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature. 1990 Aug 9;346(6284):558–560. [PubMed]
  • Breeuwer JA, Werren JH. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics. 1993 Oct;135(2):565–574. [PMC free article] [PubMed]
  • Fujii Y, Kageyama D, Hoshizaki S, Ishikawa H, Sasaki T. Transfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Proc Biol Sci. 2001 Apr 22;268(1469):855–859. [PMC free article] [PubMed]
  • Hoshizaki S, Shimada T. PCR-based detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural populations of Laodelphax striatellus (Homoptera: Delphacidae) in central Japan: has the distribution of Wolbachia spread recently? Insect Mol Biol. 1995 Nov;4(4):237–243. [PubMed]
  • Hurst GDD, Jiggins FM, Schulenburg J H G von der, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN. Male-killing Wolbachia in two species of insect. Proc Biol Sci. 1999 Apr 7;266(1420):735–735. [PMC free article]
  • Jiggins FM, von Der Schulenburg JH, Hurst GD, Majerus ME. Recombination confounds interpretations of Wolbachia evolution. Proc Biol Sci. 2001 Jul 7;268(1474):1423–1427. [PMC free article] [PubMed]
  • Rousset F, Solignac M. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6389–6393. [PMC free article] [PubMed]
  • Rousset F, Braig HR, O'Neill SL. A stable triple Wolbachia infection in Drosophila with nearly additive incompatibility effects. Heredity (Edinb) 1999 Jun;82(Pt 6):620–627. [PubMed]
  • Lassy CW, Karr TL. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech Dev. 1996 Jun;57(1):47–58. [PubMed]
  • Sinkins SP, Braig HR, O'Neill SL. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc Biol Sci. 1995 Sep 22;261(1362):325–330. [PubMed]
  • Magnin M, Pasteur N, Raymond M. Multiple incompatibilities within populations of Culex pipiens L. in southern France. Genetica. 1987 Oct 15;74(2):125–130. [PubMed]
  • Masui S, Kamoda S, Sasaki T, Ishikawa H. The first detection of the insertion sequence ISW1 in the intracellular reproductive parasite Wolbachia. Plasmid. 1999 Jul;42(1):13–19. [PubMed]
  • Skinner SW. Son-killer: a third extrachromosomal factor affecting the sex ratio in the parasitoid wasp, Nasonia (=Mormoniella) vitripennis. Genetics. 1985 Apr;109(4):745–759. [PMC free article] [PubMed]
  • Masui S, Kamoda S, Sasaki T, Ishikawa H. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J Mol Evol. 2000 Nov;51(5):491–497. [PubMed]
  • Masui S, Kuroiwa H, Sasaki T, Inui M, Kuroiwa T, Ishikawa H. Bacteriophage WO and virus-like particles in Wolbachia, an endosymbiont of arthropods. Biochem Biophys Res Commun. 2001 May 25;283(5):1099–1104. [PubMed]
  • Sasaki T, Ishikawa H. Transinfection of Wolbachia in the mediterranean flour moth, Ephestia kuehniella, by embryonic microinjection. Heredity (Edinb) 2000 Aug;85(Pt 2):130–135. [PubMed]
  • Stouthamer R, Breeuwer JA, Hurst GD. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. [PubMed]
  • Merçot H, Llorente B, Jacques M, Atlan A, Montchamp-Moreau C. Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics. 1995 Nov;141(3):1015–1023. [PMC free article] [PubMed]
  • Turelli M, Hoffmann AA. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature. 1991 Oct 3;353(6343):440–442. [PubMed]
  • Van Meer MM, Witteveldt J, Stouthamer R. Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Mol Biol. 1999 Aug;8(3):399–408. [PubMed]
  • O'Neill SL, Karr TL. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature. 1990 Nov 8;348(6297):178–180. [PubMed]
  • Werren JH. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. [PubMed]
  • O'Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. [PMC free article] [PubMed]
  • Werren JH, Bartos JD. Recombination in Wolbachia. Curr Biol. 2001 Mar 20;11(6):431–435. [PubMed]
  • Perrot-Minnot MJ, Guo LR, Werren JH. Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics. 1996 Jun;143(2):961–972. [PMC free article] [PubMed]
  • Werren JH, Zhang W, Guo LR. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci. 1995 Jul 22;261(1360):55–63. [PubMed]
  • Poinsot D, Bourtzis K, Markakis G, Savakis C, Merçot H. Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics. 1998 Sep;150(1):227–237. [PMC free article] [PubMed]

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