Abstract
In the adzuki bean borer, Ostrinia scapulalis, the sex ratio in most progenies is 1 : 1. Females from Wolbachia-infected matrilines, however, give rise to all-female broods when infected and to all-male broods when cured of the infection. These observations had been interpreted as Wolbachia-induced feminization of genetic males into functional females. Here, we show that the interpretation is incorrect. Females from both lines have a female karyotype with a WZ sex-chromosome constitution while males are ZZ. At the time of hatching from eggs, WZ and ZZ individuals are present at a 1 : 1 ratio in broods from uninfected, infected and cured females. In broods from Wolbachia-infected females, ZZ individuals die during larval development, whereas in those from cured females, WZ individuals die. Hence, development of ZZ individuals is impaired by Wolbachia but development of WZ females may require the presence of Wolbachia in infected matrilines. Sexual mosaics generated (i) by transfection of uninfected eggs and (ii) by tetracycline treatment of Wolbachia-infected mothers prior to oviposition were ZZ in all tissues, including typically female organs. We conclude that: (i) Wolbachia acts by manipulating the sex determination of its host; and (ii) although sexual mosaics can survive, development of a normal female is incompatible with a ZZ genotype.
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Selected References
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- Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M. E., Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A. 2001 May 15;98(11):6247–6252. doi: 10.1073/pnas.101304298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dyson E. A., Kamath M. K., Hurst G. D. D. Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity (Edinb) 2002 Mar;88(3):166–171. doi: 10.1038/sj.hdy.6800021. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1098/rspb.2001.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiroki Masato, Kato Yoshiomi, Kamito Takehiko, Miura Kazuki. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften. 2002 Apr;89(4):167–170. doi: 10.1007/s00114-002-0303-5. [DOI] [PubMed] [Google Scholar]
- Jeyaprakash A., Hoy M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
- Kageyama D., Nishimura G., Hoshizaki S., Ishikawa Y. Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity (Edinb) 2002 Jun;88(6):444–449. doi: 10.1038/sj.hdy.6800077. [DOI] [PubMed] [Google Scholar]
- Kageyama Daisuke, Nishimura Gen, Hoshizaki Sugihiko, Ishikawa Yukio. Two kinds of sex ratio distorters in a moth, Ostrinia scapulalis. Genome. 2003 Dec;46(6):974–982. doi: 10.1139/g03-083. [DOI] [PubMed] [Google Scholar]
- Kageyama Daisuke, Ohno Suguru, Hoshizaki Sugihiko, Ishikawa Yukio. Sexual mosaics induced by tetracycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis. Genome. 2003 Dec;46(6):983–989. doi: 10.1139/g03-082. [DOI] [PubMed] [Google Scholar]
- Marec F., Tothova A., Sahara K., Traut W. Meiotic pairing of sex chromosome fragments and its relation to atypical transmission of a sex-linked marker in Ephestia kuehniella (Insecta: Lepidoptera). Heredity (Edinb) 2001 Dec;87(Pt 6):659–671. doi: 10.1046/j.1365-2540.2001.00958.x. [DOI] [PubMed] [Google Scholar]
- Sahara Ken, Marec Franttisek, Eickhoff Ulrike, Traut Walther. Moth sex chromatin probed by comparative genomic hybridization (CGH). Genome. 2003 Apr;46(2):339–342. doi: 10.1139/g03-003. [DOI] [PubMed] [Google Scholar]
- Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
- Suzuki M. G., Shimada T., Kobayashi M. Absence of dosage compensation at the transcription level of a sex-linked gene in a female heterogametic insect, Bombyx mori. Heredity (Edinb) 1998 Sep;81(Pt 3):275–283. doi: 10.1046/j.1365-2540.1998.00356.x. [DOI] [PubMed] [Google Scholar]
- Sánchez L., Nöthiger R. Sex determination and dosage compensation in Drosophila melanogaster: production of male clones in XX females. EMBO J. 1983;2(4):485–491. doi: 10.1002/j.1460-2075.1983.tb01451.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Traut W., Eickhof U., Schorch J. C. Identification and analysis of sex chromosomes by comparative genomic hybridization (CGH). Methods Cell Sci. 2001;23(1-3):155–161. doi: 10.1007/978-94-010-0330-8_16. [DOI] [PubMed] [Google Scholar]
- Traut W., Marec F. Sex chromatin in lepidoptera. Q Rev Biol. 1996 Jun;71(2):239–256. doi: 10.1086/419371. [DOI] [PubMed] [Google Scholar]
- Werren J. H., Windsor D. M. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci. 2000 Jul 7;267(1450):1277–1285. doi: 10.1098/rspb.2000.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]