跳镰猛蚁：解码社会行为与衰老可塑性的模型昆虫

doi:10.12300/j.issn.1674-5817.2025.111

摘要/Abstract

摘要：

跳镰猛蚁（Harpegnathos saltator）是一类具有高度社会行为可塑性的真社会性昆虫，展现出独特的品级可逆性表型。与传统社会性蚂蚁不同，其工蚁在失去蚁后压制时，可通过一系列行为、神经及生理重编程，转变为有性工蚁（gamergate），且该过程可逆。因此，跳镰猛蚁成为研究社会等级建立与维持、行为调控和寿命可塑性的重要模型。得益于组学与成像技术的革新，跳镰猛蚁研究近年来取得了突破性进展。在社会等级转换过程中，个体在行为、神经系统活动、内分泌及基因表达水平等多个层面均呈现出高度动态和可塑的变化，揭示了环境信号如何整合为稳定的表型重编程。在寿命调控方面，跳镰猛蚁展现了与“繁殖-寿命对立”假说相矛盾的现象：繁殖个体寿命显著延长。相关研究揭示了端粒维持、表观遗传重塑、蛋白质稳态调控以及胰岛素/胰岛素样生长因子（insulin like growth factor，IGF）信号通路分叉等多重分子机制，为衰老与长寿研究提供了新视角。在社会化学通信与神经感知层面，跳镰猛蚁嗅觉系统进化显著，尤其是气味受体（odorant receptors，OR）基因家族的扩展，为其群体交互和等级维持提供了分子基础。神经肽与激素调控通路的研究也揭示了社会等级与行为状态之间的紧密联系。随着多种前沿工具的引入，如成簇规律间隔短回文重复序列（clustered regularly interspaced short palindromic repeats，CRISPR）/CRISPR相关蛋白核酸酶9（CRISPR-associated nuclease 9，Cas9）、基于绿色荧光蛋白（green fluorescent protein，GFP），钙调蛋白和M13肽的遗传编码钙指示器成像（genetically encoded calcium indicator imaging based on GFP， calmodulin， and M13 peptide，GCaMP imaging）、高通量测序的转座酶可及染色质检测（assay for transposase accessible chromatin with high-throughput sequencing，ATAC-seq）等，研究者能够在神经活动、基因调控与染色质可及性等多个层面进行更精确解析。这些工具的应用不仅推动了跳镰猛蚁社会行为和神经机制的深入研究，也为跨物种的比较提供了新手段。总体而言，跳镰猛蚁的研究框架涵盖社会行为、等级调控、寿命延长机制，以及基因表达与表观遗传重编程等多个方面。通过整合多组学与功能实验，研究者正逐步构建该物种社会可塑性与长寿机制的系统性图谱。这些成果不仅深化了人们对社会性昆虫行为和寿命调控的理解，也为人类抗衰老研究提供了潜在靶点和理论依据。

关键词: 跳镰猛蚁, 社会行为, 衰老, 可塑性, 神经生物学

Abstract:

Harpegnathos saltator (H. saltator) is a eusocial insect with highly plastic social behaviors, exhibiting a unique phenotype of caste reversibility. Unlike traditional social ants, when workers of H. saltator lose queen suppression, they can transform into gamergates through a series of behavioral, neural, and physiological reprogramming, and this transition is reversible. Therefore, H. saltator has become an important model for studying caste establishment and maintenance, behavioral regulation, and lifespan plasticity. Benefiting from innovations in omics and imaging technologies, research on H. saltator has achieved groundbreaking progress in recent years. During social caste transition, individuals exhibit highly dynamic and plastic changes in behavioral performance, neural activity, endocrine status, and gene expression levels, revealing how environmental signals are integrated into stable phenotypic reprogramming. In terms of lifespan regulation, H. saltator shows a phenomenon contradicting the "reproduction-lifespan trade-off" hypothesis: reproductive individuals have significantly extended lifespans. Related studies reveal multiple molecular mechanisms including telomere maintenance, epigenetic remodeling, proteostasis regulation, and insulin/insulin-like growth factor (IGF) signaling pathway bifurcation, providing new perspectives for aging and longevity research. At the level of social chemical communication and neural perception, the olfactory system of H. saltator shows remarkable evolution, particularly the expansion of the odorant receptors (OR) gene family, which provides a molecular basis for group interaction and caste maintenance. Studies on neuropeptides and hormone regulatory pathways also reveal close links between caste and behavioral states. With the introduction of various cutting-edge tools such as CRISPR (clustered regularly interspaced short palindromic repeats)/Cas9 (CRISPR-associated nuclease 9), genetically encoded calcium indicator imaging based on green fluorescent protein (GFP), calmodulin, and M13 peptide (GCaMP imaging), and assay for transposase accessible chromatin with high-throughput sequencing (ATAC-seq), researchers can conduct more precise analyses of neural activity, gene regulation, and chromatin accessibility. Application of these tools not only promotes in-depth research on social behaviors and neural mechanisms of H. saltator, but also provides novel approaches for cross-species comparison. Overall, the research framework of H. saltator covers social behavior, caste regulation, lifespan extension mechanisms, as well as gene expression and epigenetic reprogramming. By integrating multi-omics and functional experiments, researchers are progressively constructing a systematic map of social plasticity and longevity mechanisms of this species. These findings not only deepen our understanding of behavioral and lifespan regulation in social insects but also provide potential targets and a theoretical basis for human anti-aging research.

Key words: Harpegnathos saltator, Social behavior, Aging, Plasticity, Neurobiology

中图分类号:

Q95-33

盛李宏. 跳镰猛蚁：解码社会行为与衰老可塑性的模型昆虫[J]. 实验动物与比较医学, 2025, 45(6): 762-772. DOI: 10.12300/j.issn.1674-5817.2025.111.

SHENG Lihong. Harpegnathos saltator : A Model Insect for Decoding Plasticity of Social Behavior and Aging[J]. Laboratory Animal and Comparative Medicine, 2025, 45(6): 762-772. DOI: 10.12300/j.issn.1674-5817.2025.111.

图/表 4

图1 跳镰猛蚁生理和行为的可塑性

Figure 1 Physiological and behavioral plasticity of Harpegnathos saltator

图2 实验室条件下跳镰猛蚁社会品级转变研究模型的建立注：A，年轻工蚁；B，品级转变，红色圈标记触角鞭打与决斗行为的个体，蓝色圈标记“警戒”行为，通常发生在当被单独饲养的有性工蚁被转移至宿主蚁群时；C，产卵的有性工蚁（红色圈），红色箭头标记白色的卵；D，觅食的工蚁。

Figure 2 Establishment of a research model for caste transition in Harpegnathos saltator under laboratory conditionsNote： A， Callows； B， Caste transition， individuals marked with red circles are exhibiting antennal dueling behavior， and those marked with blue circles are performing "policing" behavior， which typically occurs when an isolated gamergate is reintroduced into the host colony； C， Egg-laying gamergate （red circle）， with the red arrow indicating white egg； D， Foraging workers.

图3 跳镰猛蚁品级转变相关分子变化示意图（修改自参考文献［14］）注：蚁后抑制性信息素的缺失解除对工蚁之间触角决斗行为的抑制，并引发多个组织中的一系列分子变化。假设模型：在预定将转变为有性工蚁的个体中，脑内基因表达的初始变化，如Gp-9的下调和Vg的上调，会引发一系列在脑内、脂肪体和卵巢中的基因表达级联变化，从而促进类似蚁后的表型（如蚁后信息素的生物合成和卵母细胞发育），并抑制工蚁特征（如觅食行为）和延长寿命。Ins是人类胰岛素的同源基因，IGF是人类IGF 1的同源基因。在跳镰猛蚁中，Ins先前被称为Ilp1，IGF先前被称为Ilp2［9，15］，在蜜蜂和毕氏卵角蚁中Ins的同源基因被称为Ilp2［16-18］。图中红色箭头表示在决斗蚂蚁中下调的分子，绿色箭头表示上调的分子。实线表示该分子的已知功能，虚线表示假设性调控关系。

Figure 3 Schematic diagram of molecular changes related to caste transition in Harpegnathos saltator （modified from reference［14］）Note： The absence of queen inhibitory pheromones relieves the suppression on antennal dueling behavior among workers and triggers a cascade of molecular changes across multiple tissues. Hypothetical model： initial gene expression changes in the destined gamergates brain， such as down-regulation of Gp-9 and up-regulation of vitellogenin， trigger a cascade of gene expression changes in the brain， fat body， and ovary that promote queen-like phenotypes， such as queen pheromone biosynthesis and oocyte development， and suppress worker-like phenotypes， such as foraging， while extending longevity. Ins is the homologous gene of human insulin， whereas IGF is the homologous gene of human IGF 1. Ins was previously known as Ilp1 and IGF as Ilp2 in H. saltator［9，15］， while the homologous gene of Ins in honeybees and clonal raider ants was called Ilp2 ［16-18］. Red arrows indicate downregulated molecules， green arrows indicate upregulated molecules in dueling ants. Solid lines represent confirmed molecule functions， while dashed lines represent hypothetical regulatory relationships.

图4 基于衰老标识汇总跳镰猛蚁品级转变过程中衰老调控机制的研究进展

Figure 4 Research advances in aging regulatory mechanisms during caste transition in Harpegnathos saltator based on aging hallmarks

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