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

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, Shanshan Pan, Xiawei Liu, Xuemei Liu, Jiahui Sun, Yan Liu, Hao Chen, Li Zheng, Liang Meng, Haorong Lu, He Zhang, Yifan Zhai, Qiye Li, Junnian Liu, Huanming Yang, Jian Wang, Xiaosong Hu, Xun Xu (), Shanshan Liu () and Hao Zheng ()
Additional contact information
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
Pei Zhang: BGI Research-Shenzhen
Denghui Li: BGI
Ruihua Zhang: BGI
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
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

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-58614-8

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