Sex-specific death in the Asian corn borer moth (Ostrinia furnacalis) infected with Wolbachia occurs across larval development

Genome

Volumn 50, Issue 7, 2007, Pages 645-652

  Sakamoto, Hironori ^a,c   Kageyama, Daisuke ^b   Hoshizaki, Sugihiko ^a   Ishikawa, Yukio ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c NONE   (Japan)

Author keywords

Feminization; Male killing; Ostrinia furnacalis; Sex specific lethality; Wolbachia

Indexed keywords

ANIMAL; ARTICLE; FEMALE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; MICROBIOLOGY; MOTH; PATHOGENICITY; SEX CHROMOSOME; SEX DIFFERENCE; WOLBACHIA;

ANIMALS; FEMALE; GENOTYPE; LARVA; MALE; MOTHS; SEX CHROMOSOMES; SEX FACTORS; WOLBACHIA;

ARTHROPODA; BACTERIA (MICROORGANISMS); CRAMBIDAE; LEPIDOPTERA; OSTRINIA FURNACALIS; OSTRINIA SCAPULALIS; VIGNA ANGULARIS; WOLBACHIA;

EID: 34948825793     PISSN: 08312796     EISSN: None     Source Type: Journal    
DOI: 10.1139/G07-041     Document Type: Article

References (40)

1. Baker, B.S., Gorman, M., and Marin, I. 1994. Dosage compensation in Drosophila. Annu. Rev. Genet. 28: 491-521. doi:10.1146/annurev.ge. 28.120194.002423.
2. Beeman, R.W., Friesen, K.S., and Denell, R.E. 1992. Maternal-effect selfish genes in flour beetles. Science (Washington, D.C.), 256: 89-92. doi:10.1126/science.1566060.
3. Bentley, J.K., Veneti, Z., Heraty, J., and Hurst, G.D.D. 2007. The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol. 5: 9. doi:10.1186/1741-7007-5-9.
4. Bourtzis, K., and Miller, T.A. 2003. Insect symbiosis. CRC Press, New York.
5. Bourtzis, K., and O'Neill, S. 1998. Wolbachia infections and arthropod reproduction - Wolbachia can cause cytoplasmic incompatibility, parthenogenesis, and feminization in many arthropods. Bioscience, 48: 287-293. doi:10.2307/1313355.
6. Charlat, S., and Merçot, H. 2001. Did Wolbachia cross the border? Trends Ecol. Evol. 16: 540-541. doi:10.1016/S0169-5347(01)02310- 2.
7. Clarke, C., Sheppard, P.M., and Scali, V. 1975. All-female broods in the butterfly Hypolimnas bolina (L.). Proc. R. Soc. Lond. B. Biol. Sci. 189: 29-37.
8. Dedeine, F., Vavre, F., Fleury, F., Loppin, B., Hochberg, M.E., and Boulétreau, M. 2001. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. U.S.A. 98: 6247-6252. doi:10.1073/pnas.101304298.
9. Dedeine, F., Vavre, F., Shoemaker, D.D., and Boulétreau, M. 2004. Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evolution, 58: 2167-2174.
10. Dunn, A.M., and Smith, J.E. 2001. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 3: 381-388. doi:10.1016/S1286-4579(01)01394-6.
11. Dyson, E.A., Kamath, M.K., and Hurst, G.D.D. 2002. Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity, 88: 166-172. doi:10.1038/sj.hdy.6800021.
12. Fujii, Y., Kageyama, D., Hoshizaki, S., Ishikawa, H., and Sasaki, T. 2001. Transinfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Proc. R. Soc. Lond. B. Biol. Sci. 268: 855-859.
13. Hirokawa, M. 1995. Studies on sex control in the silkworm, Bombyx mori. Bull. Fukushima Seric. Exp. Stn. 28: 1-104. [In Japanese with English summary.]
14. Hiroki, M., Kato, Y., Kamito, T., and Miura, K. 2002. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften, 89: 167-170. doi:10.1007/s00114-002-0303-5.
15. Hurst, G.D.D., and Jiggins, F.M. 2000. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg. Infect. Dis. 6: 329-336.
16. Hurst, G.D.D., and Majerus, M.E.N. 1993. Why do maternally inherited microorganisms kill males. Heredity, 71: 81-95.
17. Hurst, G.D.D., Jiggins, F.M., von der Schulenburg, J.H.G., Bertrand, D., West, S.A., Goriacheva, I.I., et al. 2000. Male-killing Wolbachia in two species of insect. Proc. R. Soc. Lond. B. Biol. Sci. 266: 735-740.
18. Hurst, L.D. 1991. The incidences and evolution of cytoplasmic male killers. Proc. R. Soc. Lond. B. Biol. Sci. 244: 91-99.
19. Hurst, L.D. 1993. The incidences, mechanisms and evolution of cytoplasmic sex-ratio distorters in animals. Biol. Rev. 68: 121-194.
20. Jiggins, F.M., Hurst, G.D.D., Dolman, C.E., and Majerus, M.E.N. 2000. High-prevalence male-killing Wolbachia in the butterfly Acraea encedana. J. Evol. Biol. 13: 495-501. doi:10.1046/j.1420-9101.2000. 00180.x.
21. Kageyama, D., and Traut, W. 2004. Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc. R. Soc. Lond. B. Biol. Sci. 271: 251-258.
22. Kageyama, D., Hoshizaki, S., and Ishikawa, Y. 1998. Female-biased sex ratio in the Asian corn borer, Ostrinia furnacalis: evidence for the occurrence of feminizing bacteria in an insect. Heredity, 81: 311-316. doi:10.1046/j.1365-2540.1998.00391.x.
23. Kageyama, D., Nishimura, G., Hoshizaki, S., and Ishikawa, Y. 2002. Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity, 88: 444-449. doi:10.1038/sj.hdy. 6800077.
24. Kageyama, D., Nishimura, G., Hoshizaki, S., and Ishikawa, Y. 2003. Sexual mosaics induced by tetracycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis. Genome, 46: 983-989. doi:10.1139/g03-082.
25. Kageyama, D., Anbutsu, H., Shimada, M., and Fukatsu, T. 2007. Spiroplasma infection causes either early or late male killing in Drosophila, depending on maternal host age. Naturwissenschaften, 94: 333-337. doi:10.1007/s00114-006-0195-x.
26. Marin, I., Siegal, M.L., and Baker, B.S. 2000. The evolution of dosage-compensation mechanisms. Bioessays, 22: 1106-1114. doi:10.1002/1521-1878(200012)22:12〈1106::AID-BIES8〉3.0. CO;2-W.
27. Mitsuhashi, W., Fukuda, H., Nicho, K., and Murakami, R. 2004. Male-killing Wolbachia in the butterfly Hypolimnas bolina. Entomol. Exp. Appl. 112: 57-64. doi:10.1111/j.0013-8703.2004.00179.x.
28. O'Neill, S.L., Giordano, R., Colbert, A.M.E., Karr, T.L.Z., and Robertson, H.M. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. U.S.A. 89: 2699-2702. doi:10.1073/pnas.89.7.2699.
29. O' Neill, S.L., Hoffman, A.A., and Werren, J.H. 1997. Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, New York.
30. Pannebakker, B.A., Loppin, B., Elemans, C.P.H., Humblot, L., and Vavre, F. 2007. Parasitic inhibition of cell death facilitates symbiosis. Proc. Natl. Acad. Sci. U.S.A. 104: 213-215. doi:10.1073/pnas.0607845104.
31. Sakamoto, H. 2006. Studies on the reproductive alteration induced by Wolbachia infection in the genus Ostrinia (Lepidoptera: Crambidae). Ph.D. thesis, University of Tokyo, Japan.
32. Sasaki, T., and Ishikawa, H. 1999. Wolbachia infections and cytoplasmic incompatibility in the almond moth and the Mediterranean flour moth. Zool. Sci. (Tokyo), 16: 739-744.
33. Schütt, C., and Nöthiger, R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development, 127: 667-677.
34. Steinmann-Zwicky, M., Amrein, H., and Nothiger, R. 1990. Genetic control of sex determination in Drosophila. Adv. Genet. 27: 189-237.
35. Stouthamer, R., Breeuwer, J.A.J., and Hurst, G.D.D. 1999. Wolbachia pipientis: microbial manipulation of arthropod reproduction. Annu. Rev. Microbiol. 53: 71-102. doi:10.1146/annurev.micro.53.1.71.
36. Suzuki, M.G., Shimada, T., and Kobayashi, M. 1998. Absence of dosage compensation at the transcription level of a sex-linked gene in a female heterogametic insect, Bombyx mori. Heredity, 81: 275-283. doi:10.1046/j.1365-2540.1998.00356.x.
37. Suzuki, M.G., Shimada, T., and Kobayashi, M. 1999. Bmkettin, homologue of the Drosophila kettin gene, is located on the Z chromosome in Bombyx mori and is not dosage compensated. Heredity, 82: 170-179. doi:10.1038/sj.hdy.6884570.
38. Tazima, Y. 1964. The genetics of the silkworm. Logos Press, London and Englewood Cliffs, N.J.
39. Traut, W., and Marec, F. 1996. Sex chromatin in lepidoptera. Q. Rev. Biol. 71: 239-256.
40. Werren, J.H. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609. doi:10.1146/annurev.ento.42.1.587.