Understanding how genotypic variation results in phenotypic variation is especially difficult for collective behaviour because group phenotypes arise from complex interactions among group members. A genome-wide association study identified hundreds of genes associated with colony-level variation in honeybee aggression, many of which also showed strong signals of positive selection, but the influence of these ‘colony aggression genes’ on brain function was unknown. Here we use single-cell (sc) transcriptomics and gene regulatory network (GRN) analyses to test the hypothesis that genetic variation for colony aggression influences individual differences in brain gene expression and/or gene regulation. We compared soldiers, which respond to territorial intrusion with stinging attacks, and foragers, which do not. Colony environment showed stronger influences on soldier-forager differences in brain gene regulation compared with brain gene expression. GRN plasticity was strongly associated with colony aggression, with larger differences in GRN dynamics detected between soldiers and foragers from more aggressive relative to less aggressive colonies. The regulatory dynamics of subnetworks composed of genes associated with colony aggression genes were more strongly correlated with each other across different cell types and brain regions relative to other genes, especially in brain regions involved with olfaction and vision and multimodal sensory integration, which are known to mediate bee aggression. These results show how group genetics can shape a collective phenotype by modulating individual brain gene regulatory network architecture.

了解基因型变异如何导致表型变异对于集体行为来说尤其困难，因为群体表型是由群体成员之间复杂的相互作用产生的。一项全基因组关联研究发现了数百个与蜜蜂攻击行为的群体水平变异相关的基因，其中许多也显示出强烈的正选择信号，但这些“群体攻击基因”对大脑功能的影响尚不清楚。在这里，我们使用单细胞（sc）转录组学和基因调控网络（GRN）分析来检验群体攻击性遗传变异影响大脑基因表达和/或基因调控个体差异的假设。我们比较了用螫刺攻击来应对领土入侵的士兵和不这样做的觅食者。与大脑基因表达相比，群体环境对士兵-采集者大脑基因调控差异的影响更大。GRN 可塑性与群体攻击性密切相关，相对于攻击性较小的群体，攻击性较强的群体的士兵和觅食者之间的 GRN 动态差异较大。相对于其他基因，由与群体攻击基因相关的基因组成的子网络的调节动态在不同的细胞类型和大脑区域中彼此之间的相关性更强，特别是在涉及嗅觉和视觉以及多模态感觉统合的大脑区域中，这些区域已知调解蜜蜂的攻击行为。这些结果表明群体遗传学如何通过调节个体大脑基因调控网络结构来塑造集体表型。