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Background <p>The domestication of transposable elements is a key source of evolutionary innovation, yet the pathways by which their functional modules are repurposed by the host remain poorly understood. The <i>Tc1/mariner</i> superfamily is a widespread group of DNA transposons, but the prevalence and patterns of their domestication are underexplored.</p> Results <p>We performed a systematic genomic screen across 43 drosophilid species using stringent criteria for molecular domestication. This analysis identified five high-confidence, evolutionarily conserved genes derived from <i>Tc1/mariner</i> transposases<i>.</i> Phylogenetic and structural analyses suggest domestication via two distinct molecular pathways: co-option of the DNA-binding module and co-option of the catalytic domain. The DNA-binding module pathway includes <i>CG4570</i>, the previously known genes <i>cag</i> and <i>toy</i> (the latter fused with a homeodomain), and a lineage-restricted gene in the <i>Drosophila obscura</i> group that exhibits signatures of recent domestication. In contrast, the catalytic domain pathway is represented solely by <i>CG14478</i>. Structural modeling reveals that CG14478 protein preserves a canonical DDE endonuclease fold. Co-expression network analysis suggests potential cellular roles of these genes: <i>CG14478</i> is linked to RNA/chromatin-related processes, <i>CG4570</i> to cell cycle/chromosome functions, <i>cag</i> to ciliary and nuclear functions, and <i>toy</i> to neuronal development.</p> Conclusions <p>This study establishes a stringent framework for identifying domesticated TEs, demonstrating that <i>Tc1/mariner</i> elements are co-opted via two distinct pathways: retention of either catalytic or DNA-binding modules. Our findings suggest that domestication is a dynamic continuum, ranging from recent, lineage-specific events to ancient, conserved genes, and underscore how genomic conflict with TEs can drive eukaryotic evolution and regulatory complexity.</p>

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Evidence for dual pathways of Tc1/mariner domestication in Drosophila

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年6月16日

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  • Iuliia O. Guseva,
  • Alexander P. Rezvykh,
  • Elena S. Zelentsova,
  • Dina A. Kulikova,
  • Michael B. Evgen’ev,
  • Sergei Y. Funikov

摘要

Background

The domestication of transposable elements is a key source of evolutionary innovation, yet the pathways by which their functional modules are repurposed by the host remain poorly understood. The Tc1/mariner superfamily is a widespread group of DNA transposons, but the prevalence and patterns of their domestication are underexplored.

Results

We performed a systematic genomic screen across 43 drosophilid species using stringent criteria for molecular domestication. This analysis identified five high-confidence, evolutionarily conserved genes derived from Tc1/mariner transposases. Phylogenetic and structural analyses suggest domestication via two distinct molecular pathways: co-option of the DNA-binding module and co-option of the catalytic domain. The DNA-binding module pathway includes CG4570, the previously known genes cag and toy (the latter fused with a homeodomain), and a lineage-restricted gene in the Drosophila obscura group that exhibits signatures of recent domestication. In contrast, the catalytic domain pathway is represented solely by CG14478. Structural modeling reveals that CG14478 protein preserves a canonical DDE endonuclease fold. Co-expression network analysis suggests potential cellular roles of these genes: CG14478 is linked to RNA/chromatin-related processes, CG4570 to cell cycle/chromosome functions, cag to ciliary and nuclear functions, and toy to neuronal development.

Conclusions

This study establishes a stringent framework for identifying domesticated TEs, demonstrating that Tc1/mariner elements are co-opted via two distinct pathways: retention of either catalytic or DNA-binding modules. Our findings suggest that domestication is a dynamic continuum, ranging from recent, lineage-specific events to ancient, conserved genes, and underscore how genomic conflict with TEs can drive eukaryotic evolution and regulatory complexity.