Traniello Ian M, Avalos Arian, Gachomba Michael J M, Gernat Tim, Chen Zhenqing, Cash-Ahmed Amy C, Hamilton Adam R, Cook Jennifer L, Robinson Gene E
Carl R Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America.
United States of America Department of Agriculture - Agricultural Research Services, Honey Bee Breeding, Genetics and Physiology Research Laboratory, Baton Rouge, Louisiana, United States of America.
PLoS Biol. 2025 Sep 16;23(9):e3003367. doi: 10.1371/journal.pbio.3003367. eCollection 2025 Sep.
Individual variation in sociability is a central feature of every society. This includes honey bees, with some individuals well connected and sociable, and others at the periphery of their colony's social network. However, the genetic and molecular bases of sociability are poorly understood. Trophallaxis-a behavior involving sharing liquid with nutritional and signaling properties-comprises a social interaction and a proxy for sociability in honey bee colonies: more sociable bees engage in more trophallaxis. Here, we identify genetic and molecular mechanisms of trophallaxis-based sociability by combining genome sequencing, brain transcriptomics, and automated behavioral tracking. A genome-wide association study (GWAS) identified 18 single nucleotide polymorphisms (SNPs) associated with variation in sociability. Several SNPs were localized to genes previously associated with sociability in other species, including in the context of human autism, suggesting shared molecular mechanisms of sociability. Variation in sociability also was linked to differential brain gene expression, particularly genes associated with neural signaling and development. Using comparative genomic and transcriptomic approaches, we also detected evidence for divergent mechanisms underpinning sociability across species, including those related to reward sensitivity and encounter probability. These results highlight both potential evolutionary conservation of the molecular roots of sociability and points of divergence.
社交能力的个体差异是每个社会的核心特征。这包括蜜蜂,有些个体社交广泛且善于社交,而另一些则处于蜂群社交网络的边缘。然而,社交能力的遗传和分子基础却鲜为人知。交哺行为——一种涉及分享具有营养和信号特性液体的行为——构成了蜜蜂群体中的一种社会互动和社交能力的代表:更善于社交的蜜蜂参与更多的交哺行为。在这里,我们通过结合基因组测序、脑转录组学和自动行为跟踪,确定了基于交哺行为的社交能力的遗传和分子机制。全基因组关联研究(GWAS)确定了18个与社交能力变异相关的单核苷酸多态性(SNP)。几个SNP定位于先前在其他物种中与社交能力相关的基因,包括在人类自闭症的背景下,这表明社交能力存在共同的分子机制。社交能力的变异也与大脑基因表达差异有关,特别是与神经信号传导和发育相关的基因。使用比较基因组和转录组方法,我们还检测到不同物种间社交能力背后存在不同机制的证据,包括与奖励敏感性和相遇概率相关的机制。这些结果突出了社交能力分子根源的潜在进化保守性和差异点。