Sexual mosaics induced by tetracycline treatment in the <i>Wolbachia</i>-infected adzuki bean borer, <i>Ostrinia scapulalis</i>

Kageyama, Daisuke; Ohno, Suguru; Hoshizaki, Sugihiko; Ishikawa, Yukio

doi:10.1139/g03-082

Cited by 28 publications

(26 citation statements)

References 9 publications

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“…B (2004) that is necessary for female survival or female sex determination may have lost its function by mutation while Wolbachia was performing that function. Fujii et al (2001) (c) The mechanism of sex-specific interference Incomplete curing of Wolbachia results in the development of sexual-mosaic individuals (Kageyama et al 2003b). We show here that the mosaics are not genetic mosaics but genetically homogeneous male individuals.…”

Section: Discussion (A) Wz-zz Sex-chromosome Systemmentioning

confidence: 81%

Opposite sex–specific effects ofWolbachiaand interference with the sex determination of its hostOstrinia scapulalis

Kageyama

Traut

2004

Proc. R. Soc. Lond. B

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103

131

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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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Section: Discussion (A) Wz-zz Sex-chromosome Systemmentioning

confidence: 81%

Opposite sex–specific effects ofWolbachiaand interference with the sex determination of its hostOstrinia scapulalis

Kageyama

Traut

2004

Proc. R. Soc. Lond. B

Self Cite

103

131

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“…The elimination of Wolbachia from infected strains of O. scapulalis by tetracycline treatment, curiously, gave rise to all-male progeny, suggesting that Wolbachia is indispensable for the development of females in the infected strains (Kageyama and Traut, 2004). Interestingly, when Wolbachia-infected female moths were treated with tetracycline prior to oviposition, they often produced genetically male moths with sexually mosaic phenotypes (Kageyama et al, 2003b;Kageyama and Traut, 2004). This finding demonstrates that the Wolbachia strain in O. scapulalis has a feminizing effect on genetic males.…”

Section: Introductionmentioning

confidence: 94%

Expression of a doublesex homologue is altered in sexual mosaics of Ostrinia scapulalis moths infected with Wolbachia

Sugimoto

Fujii

Kayukawa

et al. 2010

Insect Biochemistry and Molecular Biology

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“…Intersexuality has been observed in various lepidopteran insects, such as the gypsy moth, Lymantria dispar (11,32), the bagworm, Solenobia triquetrella (43,44), the adzuki bean borer, Ostrinia scapulalis (22,23), the silkworm, Bombyx mori (16), and others. In O. scapulalis, intersexual individuals with sexually mosaic phenotypes were induced by antibiotic treatment of Wolbachia-infected insects (22,23). Timing of antibiotic treatment and expression of sexually intermediate traits.…”

Section: Vol 73 2007 Wolbachia-induced Feminization In a Butterfly mentioning

confidence: 99%

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

Narita

Kageyama

Nomura

et al. 2007

Appl Environ Microbiol

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126

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When the butterfly Eurema hecabe is infected with two different strains (wHecCI2 and wHecFem2) of the bacterial endosymbiont Wolbachia, genetic males are transformed into functional females, resulting in production of all-female broods. In an attempt to understand how and when the Wolbachia endosymbiont feminizes genetically male insects, larval insects were fed an antibiotic-containing diet beginning at different developmental stages until pupation. When the adult insects emerged, strikingly, many of them exhibited sexually intermediate traits in their wings, reproductive organs, and genitalia. The expression of intersexual phenotypes was strong in the insects treated from first instar, moderate in the insects treated from third instar, and weak in the insects treated from fourth instar. The insects treated from early larval instar grew and pupated normally but frequently failed to emerge and died in the pupal case. The dead insects in the pupal case contained lower densities of the feminizing Wolbachia endosymbiont than the successfully emerged insects, although none of them were completely cured of the symbiont infection. These results suggest the following: (i) the antibiotic treatment suppressed the population of feminizing Wolbachia endosymbionts; (ii) the suppression probably resulted in attenuated feminizing activity of the symbiont, leading to expression of intersexual host traits; (iii) many of the insects suffered pupal mortality, possibly due to either intersexual defects or Wolbachia-mediated addiction; and hence (iv) the feminizing Wolbachia endosymbiont continuously acts on the host insects during larval development for expression of female phenotypes under a male genotype. Our finding may prompt reconsideration of the notion that Wolbachia-induced reproductive manipulations are already complete before the early embryonic stage and provide insights into the mechanism underlying the symbiontinduced reversal of insect sex.

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Sexual mosaics induced by tetracycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis

Cited by 28 publications

References 9 publications

Opposite sex–specific effects ofWolbachiaand interference with the sex determination of its hostOstrinia scapulalis

Opposite sex–specific effects ofWolbachiaand interference with the sex determination of its hostOstrinia scapulalis

Expression of a doublesex homologue is altered in sexual mosaics of Ostrinia scapulalis moths infected with Wolbachia

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

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