The brain atlas of a subsocial bee reflects that of eusocial Hymenoptera

IF 2.4 4区 心理学 Q2 BEHAVIORAL SCIENCES Genes Brain and Behavior Pub Date : 2024-11-08 DOI:10.1111/gbb.70007
Benjamin C. Pyenson, Jesse L. Huisken, Nandini Gupta, Sandra M. Rehan
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Abstract

The evolutionary transition from solitary life to group-living in a society with cooperative brood care, reproductive division of labor and morphological castes is associated with increased cognitive demands for task-specialization. Associated with these demands, the brains of eusocial Hymenoptera divide transcriptomic signatures associated with foraging and reproduction to different populations of cells and also show diverse astrocyte and Kenyon cell types compared with solitary non-hymenopteran insects. The neural architecture of subsocial bees, which represent evolutionary antecedent states to eusocial Hymenoptera, could then show how widely this eusocial brain is conserved across aculeate Hymenoptera. Using single-nucleus transcriptomics, we have created an atlas of neuron and glial cell types from the brain of a subsocial insect, the small carpenter bee (Ceratina calcarata). The proportion of C. calcarata neurons related to the metabolism of classes of neurotransmitters is similar to that of other insects, whereas astrocyte and Kenyon cell types show highly similar gene expression patterns to those of eusocial Hymenoptera. In the winter, the transcriptomic signature across the brain reflected diapause. When the bee was active in the summer, however, genes upregulated in neurons reflected foraging, while the gene expression signature of glia associated with reproductive functions. Like eusocial Hymenoptera, we conclude that neural components for foraging and reproduction in C. calcarata are compartmentalized to different parts of its brain. Cellular examination of the brains of other solitary and subsocial insects can show the extent of neurobiological conservation across levels of social complexity.

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亚社会性蜜蜂的脑图谱反映了优社会性膜翅目昆虫的脑图谱。
在具有合作育雏、生殖分工和形态种姓的社会中,从独居到群居的进化过渡与任务专业化的认知需求增加有关。与这些要求有关,与独居的非膜翅目昆虫相比,群居膜翅目昆虫的大脑将与觅食和繁殖有关的转录组特征划分到不同的细胞群中,并显示出不同的星形胶质细胞和凯尼恩细胞类型。亚社会性蜜蜂代表了单社会性膜翅目昆虫的进化前身状态,它们的神经结构可以显示单社会性大脑在微体膜翅目昆虫中的广泛保守性。利用单核转录组学,我们绘制了亚社会性昆虫--小木匠蜂(Ceratina calcarata)大脑神经元和神经胶质细胞类型图谱。小木匠蜂神经元中与神经递质类代谢相关的比例与其他昆虫相似,而星形胶质细胞和肯尼恩细胞类型的基因表达模式与雌性膜翅目昆虫高度相似。在冬季,整个大脑的转录组特征反映出蜜蜂处于休眠状态。然而,当蜜蜂在夏季活动时,神经元中上调的基因反映了觅食功能,而神经胶质细胞的基因表达特征则与生殖功能有关。与群居膜翅目昆虫一样,我们得出结论:钙蜂的觅食和繁殖神经成分被分隔在大脑的不同部位。对其他独居昆虫和亚社会昆虫大脑的细胞检查可以显示不同社会复杂程度的神经生物学保护程度。
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来源期刊
Genes Brain and Behavior
Genes Brain and Behavior 医学-行为科学
CiteScore
6.80
自引率
4.00%
发文量
62
审稿时长
4-8 weeks
期刊介绍: Genes, Brain and Behavior was launched in 2002 with the aim of publishing top quality research in behavioral and neural genetics in their broadest sense. The emphasis is on the analysis of the behavioral and neural phenotypes under consideration, the unifying theme being the genetic approach as a tool to increase our understanding of these phenotypes. Genes Brain and Behavior is pleased to offer the following features: 8 issues per year online submissions with first editorial decisions within 3-4 weeks and fast publication at Wiley-Blackwells High visibility through its coverage by PubMed/Medline, Current Contents and other major abstracting and indexing services Inclusion in the Wiley-Blackwell consortial license, extending readership to thousands of international libraries and institutions A large and varied editorial board comprising of international specialists.
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