Single-nucleus and spatial transcriptomics identify brain landscape of gene regulatory networks associated with behavioral maturation in honeybees
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.
Authors
- Huanming Yang (ORCID: https://orcid.org/0000-0002-0858-3410)
- Haorong Lu (ORCID: https://orcid.org/0000-0003-0132-8166)
- Qianyue Ji (ORCID: https://orcid.org/0000-0001-9311-360X)
- Li Zheng (ORCID: https://orcid.org/0000-0002-7033-4802)
- Yifan Zhai (ORCID: https://orcid.org/0000-0002-6303-2056)
- Yating Qin (ORCID: https://orcid.org/0000-0001-8024-3210)
- Qiye Li (ORCID: https://orcid.org/0000-0002-5993-0312)
- Xiaohuan Mu (ORCID: https://orcid.org/0000-0003-4363-6052)
- Xiao Hu (ORCID: https://orcid.org/0000-0003-1128-4099)
- Jianwu Wang (ORCID: https://orcid.org/0000-0002-4421-8058)
- Zijing Zhang (ORCID: https://orcid.org/0000-0002-6446-5486)
- Junnian Liu
- Denghui Li (ORCID: https://orcid.org/0009-0009-5326-9955)
- Qunfei Guo (ORCID: https://orcid.org/0000-0001-8530-3649)
- Jie Ma (ORCID: https://orcid.org/0000-0001-6765-2394)
- Nannan Zhang (ORCID: https://orcid.org/0000-0001-6747-8920)
- Hao Zheng (ORCID: https://orcid.org/0000-0003-3313-1675)
- Qun Liu (ORCID: https://orcid.org/0000-0002-0111-4849)
- Haoyu Lang (ORCID: https://orcid.org/0000-0003-4983-4543)
- Yang Wang (ORCID: https://orcid.org/0000-0003-0447-3107)
- Yan Liu
- Hao Chen
- Pei Zhang (ORCID: https://orcid.org/0000-0003-2054-928X)
- Shanshan Liu (ORCID: https://orcid.org/0000-0003-4677-9948)
- Xuemei Liu (ORCID: https://orcid.org/0000-0003-0201-277X)
- He Zhang (ORCID: https://orcid.org/0000-0001-9294-1403)
- Xun Xu (ORCID: https://orcid.org/0000-0002-5338-5173)
- Liang Meng (ORCID: https://orcid.org/0000-0002-6238-7939)
- Ruihua Zhang (ORCID: https://orcid.org/0000-0002-8672-9673)
- Shan-Shan Pan
- Yingying Zhang (ORCID: https://orcid.org/0000-0001-9796-919X)
- Jiahui Sun (ORCID: https://orcid.org/0000-0002-6192-9679)
- Aijun Jiang
- Xiawei Liu
Institutions
- BGI Group (China) (CN)
- Institute of Plant Protection (CN)
- Shandong Academy of Agricultural Sciences (CN)
- University of Chinese Academy of Sciences (CN)
- BGI Research (CN)
- China Agricultural University (CN)
- Hebei Normal University (CN)
Publication Details
- Journal
- Nature Communications
- Published
- 2025-04-08
- DOI
- https://doi.org/10.1038/s41467-025-58614-8
- Citations
- 7
- Primary Topic
- Insect and Arachnid Ecology and Behavior
- Type
- article
- Field-Weighted Citation Impact
- 12.72
Funders
- National Natural Science Foundation of China
- National Science Fund for Distinguished Young Scholars