Many eusocial insects can distinguish nestmates from non-nestmate conspecifics, which ensures that altruistic behavior is directed toward close relatives. In termites, however, colonies exhibit various responses to non-nestmates: from killing to accepting as a colony member. Why and how termite colonies adopt closed versus open societies remain largely unknown, while it is presumably related to not only genetic but also social-environmental factors. Here, we show that kings and queens play a key role in maintaining high aggression levels of workers and soldiers toward non-nestmate intruders in the subterranean termite Reticulitermes speratus. The level of aggression toward non-nestmate conspecifics was significantly lower in “royal-absent” colonies compared to “royal-present” colonies. In addition, the proportion of workers and soldiers exhibiting aggressive behaviors toward non-nestmates decreased in the absence of kings and queens. Our results demonstrate that social conditions, including royal presence, can influence intercolonial interactions, and may explain why previous studies of termite aggression have reported contradictory findings. This study provides important new insights into nestmate recognition and colony defense in eusocial insects.

许多亲社会的昆虫可以将巢生与非巢生的种区分开，这确保了利他行为是针对近亲的。然而，在白蚁中，殖民地对非巢穴表现出各种反应：从杀死到成为殖民地成员。白蚁群体为什么采用封闭社会还是采用开放社会，以及如何采用封闭社会，目前仍不得而知，尽管它不仅与遗传因素有关，而且与社会环境因素有关。在这里，我们表明国王和王后在维持工蚁和士兵对地下白蚁Reticulitermes speratus的非巢穴入侵者的高侵略性中起关键作用。。与“王室存在”菌落相比，“无王室”菌落对非巢状同种菌的侵袭水平明显更低。此外，在没有国王和王后的情况下，对非牧师表现出侵略行为的工人和士兵的比例下降了。我们的结果表明，包括王室成员的存在在内的社会条件可能会影响殖民地之间的互动，并且可以解释为什么先前对白蚁侵略的研究报告了矛盾的发现。这项研究提供了重要的新见解，以了解真社会昆虫中的巢穴识别和菌落防御。