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Single-nucleus and spatial transcriptomics identify brain landscape of gene regulatory networks associated with behavioral maturation in honeybees

Author

Listed:
  • Xiaohuan Mu

    (China Agricultural University)

  • Zijing Zhang

    (Hebei Normal University)

  • Qun Liu

    (BGI)

  • Jie Ma

    (BGI)

  • Yating Qin

    (BGI)

  • Haoyu Lang

    (China Agricultural University)

  • Yingying Zhang

    (BGI)

  • Nannan Zhang

    (BGI)

  • Qunfei Guo

    (BGI Research-Shenzhen
    University of Chinese Academy of Sciences)

  • Pei Zhang

    (BGI Research-Shenzhen)

  • Denghui Li

    (BGI)

  • Ruihua Zhang

    (BGI
    University of Chinese Academy of Sciences)

  • Qianyue Ji

    (BGI)

  • Aijun Jiang

    (BGI)

  • Yang Wang

    (BGI Research-Shenzhen)

  • Shanshan Pan

    (BGI)

  • Xiawei Liu

    (BGI)

  • Xuemei Liu

    (BGI)

  • Jiahui Sun

    (BGI)

  • Yan Liu

    (Shandong Academy of Agricultural Sciences)

  • Hao Chen

    (Shandong Academy of Agricultural Sciences)

  • Li Zheng

    (Shandong Academy of Agricultural Sciences)

  • Liang Meng

    (BGI)

  • Haorong Lu

    (BGI Research-Shenzhen)

  • He Zhang

    (BGI Research-Shenzhen)

  • Yifan Zhai

    (Shandong Academy of Agricultural Sciences)

  • Qiye Li

    (BGI Research-Shenzhen
    University of Chinese Academy of Sciences)

  • Junnian Liu

    (BGI)

  • Huanming Yang

    (BGI Research-Shenzhen)

  • Jian Wang

    (BGI Research-Shenzhen)

  • Xiaosong Hu

    (China Agricultural University)

  • Xun Xu

    (BGI Research-Shenzhen)

  • Shanshan Liu

    (BGI)

  • Hao Zheng

    (China Agricultural University)

Abstract

Animal behavior is linked to the gene regulatory network (GRN) coordinating gene expression in the brain. Eusocial honeybees, with their natural behavioral plasticity, provide an excellent model for exploring the connection between brain activity and behavior. Using single-nucleus RNA sequencing and spatial transcriptomics, we analyze the expression patterns of brain cells associated with the behavioral maturation from nursing to foraging. Integrating spatial and cellular data uncovered cell-type and spatial heterogeneity in GRN organization. Interestingly, the stripe regulon is explicitly activated in foragers’ small Keyon cells, which are implicated in spatial learning and navigation. When worker age is controlled in artificial colonies, stripe and its key targets remained highly expressed in the KC regions of bees performing foraging tasks. These findings suggest that specific GRNs coordinate individual brain cell activity during behavioral transitions, shedding light on GRN-driven brain heterogeneity and its role in the division of labor of social life.

Suggested Citation

  • Xiaohuan Mu & Zijing Zhang & Qun Liu & Jie Ma & Yating Qin & Haoyu Lang & Yingying Zhang & Nannan Zhang & Qunfei Guo & Pei Zhang & Denghui Li & Ruihua Zhang & Qianyue Ji & Aijun Jiang & Yang Wang & Sh, 2025. "Single-nucleus and spatial transcriptomics identify brain landscape of gene regulatory networks associated with behavioral maturation in honeybees," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58614-8
    DOI: 10.1038/s41467-025-58614-8
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    References listed on IDEAS

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