<p>Sexual dimorphism represents a striking dimension of morphological diversity both within and across taxa. Female-specific wing regression (FSWR) is common in insects, but the mechanisms underlying this regression remain largely unknown. Here we show that FSWR is widespread among Pterygota insects, including cockroaches, where it contributes to ecological adaptation. We reveal that FSWR regulation involves sex-specific isoforms of DSX, a master regulator in the insect sex differentiation pathway, which oppositely regulate the expression of <i>E93</i>, the insect metamorphosis-controlling ‘adult factor’, during wing development. Mechanistically, DSX<sup>F</sup> represses, while DSX<sup>M</sup> activates, <i>E93</i> expression through binding to DSX-binding motifs in FSWR lineages. This differential binding remodels chromatin accessibility and establishes a male-specific three-dimensional topology, facilitating the formation of an enhancer–promoter loop. Consequently, wing morphogenesis gene expression and wing blade cell type specification are promoted in males but suppressed in females. Taken together, our findings provide mechanistic insights into how the rewiring of two conserved signalling hubs into one axis can create regulatory degrees of freedom, thereby generating novel phenotypic variation able to fuel the exploitation of new ecological niches.</p>

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Rewiring of two conserved signalling hubs into one axis underlies convergent female-specific wing regression in insects

  • Mingtao Liao,
  • Xinyi Chen,
  • Dong Zhao,
  • Dongwei Yuan,
  • Danyan Huang,
  • Ziyu Yan,
  • Liangqiong Huang,
  • Jiaxin Ni,
  • Qing Ma,
  • Yufeng Pan,
  • Yonggang Hu,
  • Armin P. Moczek,
  • Wei Zhang,
  • Chonghua Ren,
  • Sheng Li

摘要

Sexual dimorphism represents a striking dimension of morphological diversity both within and across taxa. Female-specific wing regression (FSWR) is common in insects, but the mechanisms underlying this regression remain largely unknown. Here we show that FSWR is widespread among Pterygota insects, including cockroaches, where it contributes to ecological adaptation. We reveal that FSWR regulation involves sex-specific isoforms of DSX, a master regulator in the insect sex differentiation pathway, which oppositely regulate the expression of E93, the insect metamorphosis-controlling ‘adult factor’, during wing development. Mechanistically, DSXF represses, while DSXM activates, E93 expression through binding to DSX-binding motifs in FSWR lineages. This differential binding remodels chromatin accessibility and establishes a male-specific three-dimensional topology, facilitating the formation of an enhancer–promoter loop. Consequently, wing morphogenesis gene expression and wing blade cell type specification are promoted in males but suppressed in females. Taken together, our findings provide mechanistic insights into how the rewiring of two conserved signalling hubs into one axis can create regulatory degrees of freedom, thereby generating novel phenotypic variation able to fuel the exploitation of new ecological niches.