Background <p>Interspecific hybridization is a fundamental evolutionary process, yet it often results in male sterility due to genomic incompatibilities and disrupted epigenetic regulation. While fertility variation among hybrids is increasingly acknowledged, the precise mechanisms linking these molecular disruptions to reproductive outcomes in vertebrates remain underexplored.</p> Results <p>To address this, we investigated testicular chromatin dynamics and gene expression in 19 mature male F<sub>1</sub> hybrids derived from a paternal bluntnose black bream (<i>Megalobrama amblycephala</i>, BSB) and a maternal topmouth culter (<i>Culter alburnus</i>, TC). These two species diverged approximately 12.74 million years ago, and their F<sub>1</sub> hybrid offspring display a wide range of fertility. Our integrative multi-omics analysis revealed several insights into the molecular basis of hybrid fertility. Genes inherited from the BSB parent exert a disproportionate influence on reproductive outcomes, indicating an asymmetric parental contribution. Furthermore, chromatin architecture analysis showed that BSB-derived enhancer-promoter networks are characterized by longer interaction distances and greater regulatory strength, suggesting distinct subgenome-specific topologies. Then, our analysis identified the BSB-derived gene <i>LOC125267388</i> as a critical regulator of fertility. Homologous to a retrotransposon esterase and containing conserved teleost motifs, this gene likely contributes to the epigenetic modulation of hybrid fertility.</p> Conclusions <p>These findings provide insights into the chromatin-mediated mechanisms underpinning reproductive barriers in vertebrate hybrids, contributing to a deeper understanding of evolutionary divergence and hybrid incompatibility.</p>

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Chromatin-mediated mechanisms of hybrid fertility in F1 male hybrids of Culter alburnus and Megalobrama amblycephala

  • Li Ren,
  • Kai Yang,
  • Yiyan Zeng,
  • Ruyi Zhang,
  • Ling Liu,
  • Huiya Guan,
  • Jinhui Zhang,
  • Xiaohuan Han,
  • Shaojun Liu

摘要

Background

Interspecific hybridization is a fundamental evolutionary process, yet it often results in male sterility due to genomic incompatibilities and disrupted epigenetic regulation. While fertility variation among hybrids is increasingly acknowledged, the precise mechanisms linking these molecular disruptions to reproductive outcomes in vertebrates remain underexplored.

Results

To address this, we investigated testicular chromatin dynamics and gene expression in 19 mature male F1 hybrids derived from a paternal bluntnose black bream (Megalobrama amblycephala, BSB) and a maternal topmouth culter (Culter alburnus, TC). These two species diverged approximately 12.74 million years ago, and their F1 hybrid offspring display a wide range of fertility. Our integrative multi-omics analysis revealed several insights into the molecular basis of hybrid fertility. Genes inherited from the BSB parent exert a disproportionate influence on reproductive outcomes, indicating an asymmetric parental contribution. Furthermore, chromatin architecture analysis showed that BSB-derived enhancer-promoter networks are characterized by longer interaction distances and greater regulatory strength, suggesting distinct subgenome-specific topologies. Then, our analysis identified the BSB-derived gene LOC125267388 as a critical regulator of fertility. Homologous to a retrotransposon esterase and containing conserved teleost motifs, this gene likely contributes to the epigenetic modulation of hybrid fertility.

Conclusions

These findings provide insights into the chromatin-mediated mechanisms underpinning reproductive barriers in vertebrate hybrids, contributing to a deeper understanding of evolutionary divergence and hybrid incompatibility.