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Background <p>The primary signals of sex determination in insects are diverse and evolve erratically. This also appears to be the case with moths and butterflies. In the silkworm <i>Bombyx mori</i>, female development is triggered by a W chromosome-derived <i>Feminizer</i> (<i>Fem</i>) piRNA that degrades the mRNA of the Z-linked <i>Masculinizer</i> (<i>Masc</i>) gene, which controls male development. We investigated whether this mechanism is conserved in another group of Lepidoptera.</p> Results <p>We identified a putative feminizing piRNA and many partial copies of the <i>EkMasc</i> gene on the W chromosome of <i>Ephestia kuehniella</i>. The piRNA is generated by a repetitive W-linked sequence named <i>E. kuehniella Moth-overruler-of-masculinization</i> (<i>EkMom</i>). <i>EkMom</i> piRNA shows high similarity to a region of Z-linked <i>EkMasc</i> and is expressed at the onset of female development, but has no relationship to the <i>B. mori Fem</i> piRNA. We then mapped small RNA-seq data from embryos of the related <i>Plodia interpunctella</i> to the <i>PiMasc</i> gene and identified a single small RNA, a <i>PiMom</i> piRNA, able to target <i>PiMasc</i> and with high sequence identity to the <i>EkMom</i> piRNA. Both the <i>PiMom</i> and <i>EkMom</i> repeats are present in high copy number and form a single cluster on the W chromosome. In both species, the <i>Mom</i> piRNA is responsible for <i>Masc</i> mRNA cleavage, clearly demonstrating that the <i>Mom</i> piRNA triggers female development.</p> Conclusions <p>Our study provides multiple lines of evidence that <i>Mom</i> piRNA is the primary sex-determining signal in two pyralid moths and highlights a possible pathway for the origin of feminizing piRNAs in Lepidoptera. The similarity in female sex determination between the phylogenetically distant species suggests convergent evolution of feminizing piRNAs in Lepidoptera.</p>

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A W chromosome-derived feminizing piRNA in pyralid moths demonstrates convergent evolution for primary sex determination signals in Lepidoptera

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  • 发表日期：

    2025年10月1日

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  • Sander Visser,
  • Atsuo Yoshido,
  • Irena Provazníková,
  • Martina Dalíková,
  • Dagmar Voříšková,
  • Anna Chung Voleníková,
  • Eveline C. Verhulst,
  • František Marec

摘要

Background

The primary signals of sex determination in insects are diverse and evolve erratically. This also appears to be the case with moths and butterflies. In the silkworm Bombyx mori, female development is triggered by a W chromosome-derived Feminizer (Fem) piRNA that degrades the mRNA of the Z-linked Masculinizer (Masc) gene, which controls male development. We investigated whether this mechanism is conserved in another group of Lepidoptera.

Results

We identified a putative feminizing piRNA and many partial copies of the EkMasc gene on the W chromosome of Ephestia kuehniella. The piRNA is generated by a repetitive W-linked sequence named E. kuehniella Moth-overruler-of-masculinization (EkMom). EkMom piRNA shows high similarity to a region of Z-linked EkMasc and is expressed at the onset of female development, but has no relationship to the B. mori Fem piRNA. We then mapped small RNA-seq data from embryos of the related Plodia interpunctella to the PiMasc gene and identified a single small RNA, a PiMom piRNA, able to target PiMasc and with high sequence identity to the EkMom piRNA. Both the PiMom and EkMom repeats are present in high copy number and form a single cluster on the W chromosome. In both species, the Mom piRNA is responsible for Masc mRNA cleavage, clearly demonstrating that the Mom piRNA triggers female development.

Conclusions

Our study provides multiple lines of evidence that Mom piRNA is the primary sex-determining signal in two pyralid moths and highlights a possible pathway for the origin of feminizing piRNAs in Lepidoptera. The similarity in female sex determination between the phylogenetically distant species suggests convergent evolution of feminizing piRNAs in Lepidoptera.