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Applied and Environmental Microbiology, July 2007, p. 4332-4341, Vol. 73, No. 13
0099-2240/07/$08.00+0 doi:10.1128/AEM.00145-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.
Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development
Satoko Narita,1
Daisuke Kageyama,2
Masashi Nomura,1 and
Takema Fukatsu3*
Faculty of Horticulture, Chiba University, Matsudo, Chiba 271-8510, Japan,1 National Institute of Agrobiological Sciences (NIAS), Tsukuba, Ibaraki 305-8634, Japan,2 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8566, Japan3
Received 19 January 2007/ Accepted 3 May 2007
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 symbiont-induced reversal of insect sex.
* Corresponding author. Mailing address: National Institute of Advanced Industrial Science and Technology (AIST), AIST Tsukuba Central 6, Tsukuba 305-8566, Japan. Phone: 81-29-861-6087. Fax: 81-29-861-6080. E-mail: t-fukatsu{at}aist.go.jp
Published ahead of print on 11 May 2007.
Applied and Environmental Microbiology, July 2007, p. 4332-4341, Vol. 73, No. 13
0099-2240/07/$08.00+0 doi:10.1128/AEM.00145-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.
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