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<p><i>Wolbachia</i> infection causes male-specific death in <i>Ostrinia furnacalis</i>, but its removal from infected strains results in female-specific death instead of restoring 1:1 sex ratio, suggesting that cytoplasmic <i>Wolbachia</i>, not the host genome, primarily determines femaleness in infected strains. This phenomenon is a striking example of the evolutionary outcome of cytoplasmic sex determination, potentially arising from prolonged host-symbiont co-evolution. Although we recently identified Oscar, the <i>Wolbachia</i>-encoded male-killing effector targeting the host masculinizing factor OfMasc in <i>Ostrinia</i> moths, inactivation or loss of the host’s endogenous feminizer remains unknown. Here we identify a W-linked primary feminizer, <i>OfFem</i> piRNA, which targets an mRNA encoding an OfMasc-interacting protein Ofznf-2. We demonstrate that Ofznf-2 is essential for both masculinization and dosage compensation. We also show that <i>OfFem</i> piRNA is entirely absent in the <i>Wolbachia</i>-infected lineage, providing molecular evidence that a male-killing <i>Wolbachia</i> hijacks the host feminizing piRNA function by acquiring the Oscar protein during prolonged endosymbiosis.</p>

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Complete transition from chromosomal to cytoplasmic sex determination during prolonged Wolbachia symbiosis

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年1月8日

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  • Takahiro Fukui,
  • Tomohiro Muro,
  • Noriko Matsuda-Imai,
  • Tatsunori Kaneda,
  • Hidetaka Kosako,
  • Hideaki Hiraki,
  • Keisuke Shoji,
  • Takeshi Fujii,
  • Yutaka Suzuki,
  • Atsushi Toyoda,
  • Takehiko Itoh,
  • Takashi Kiuchi,
  • Susumu Katsuma

摘要

Wolbachia infection causes male-specific death in Ostrinia furnacalis, but its removal from infected strains results in female-specific death instead of restoring 1:1 sex ratio, suggesting that cytoplasmic Wolbachia, not the host genome, primarily determines femaleness in infected strains. This phenomenon is a striking example of the evolutionary outcome of cytoplasmic sex determination, potentially arising from prolonged host-symbiont co-evolution. Although we recently identified Oscar, the Wolbachia-encoded male-killing effector targeting the host masculinizing factor OfMasc in Ostrinia moths, inactivation or loss of the host’s endogenous feminizer remains unknown. Here we identify a W-linked primary feminizer, OfFem piRNA, which targets an mRNA encoding an OfMasc-interacting protein Ofznf-2. We demonstrate that Ofznf-2 is essential for both masculinization and dosage compensation. We also show that OfFem piRNA is entirely absent in the Wolbachia-infected lineage, providing molecular evidence that a male-killing Wolbachia hijacks the host feminizing piRNA function by acquiring the Oscar protein during prolonged endosymbiosis.