Department of Ecology and Evolutionary Biology, Lewis-Sigler Institute for Integrative Biology, and Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey, USA; email:
Smithsonian Tropical Research Institute, Ancon, Panama.
Annu Rev Genet. 2024 Nov;58(1):273-295. doi: 10.1146/annurev-genet-111523-102510. Epub 2024 Nov 14.
The evolution of eusociality in Hymenoptera-encompassing bees, ants, and wasps-is characterized by multiple gains and losses of social living, making this group a prime model to understand the mechanisms that underlie social behavior and social complexity. Our review synthesizes insights into the evolutionary history and molecular basis of eusociality. We examine new evidence for key evolutionary hypotheses and molecular pathways that regulate social behaviors, highlighting convergent evolution on a shared molecular toolkit that includes the insulin/insulin-like growth factor signaling (IIS) and target of rapamycin (TOR) pathways, juvenile hormone and ecdysteroid signaling, and epigenetic regulation. We emphasize how the crosstalk among these nutrient-sensing and endocrine signaling pathways enables social insects to integrate external environmental stimuli, including social cues, with internal physiology and behavior. We argue that examining these pathways as an integrated regulatory circuit and exploring how the regulatory architecture of this circuit evolves alongside eusociality can open the door to understanding the origin of the complex life histories and behaviors of this group.
膜翅目（包括蜜蜂、蚂蚁和黄蜂）中社会性的进化特征是多次获得和失去群居生活，这使得该群体成为理解支配社会行为和社会复杂性的机制的主要模型。我们的综述综合了对社会性进化历史和分子基础的见解。我们检查了关键进化假设和调控社会行为的分子途径的新证据，突出了共享分子工具包上的趋同进化，其中包括胰岛素/胰岛素样生长因子信号（IIS）和雷帕霉素靶蛋白（TOR）途径、保幼激素和蜕皮激素信号以及表观遗传调控。我们强调了这些营养感应和内分泌信号途径之间的相互作用如何使社会性昆虫能够将外部环境刺激（包括社会线索）与内部生理学和行为结合起来。我们认为，将这些途径作为一个集成的调节回路进行检查，并探索这个回路的调节结构如何随着社会性的进化而演变，可以为理解这个群体复杂的生活史和行为的起源打开大门。
