Early queen infection shapes developmental dynamics and induces long-term disease protection in incipient ant colonies

Infections early in life can have enduring effects on an organism’s development and immunity. In this study, we show that this equally applies to developing “superorganisms” – incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colonies grew more slowly than controls before winter, but reached similar sizes afterwards. Independent of exposure, queen hibernation survival improved when the ratio of pupae to workers was small. Queens that reared fewer pupae before worker emergence exhibited lower pathogen levels, indicating that high brood rearing efforts interfere with the ability of the queen’s immune system to suppress pathogen proliferation. Early-life queen pathogen-exposure also improved the immunocompetence of her worker offspring, as demonstrated by challenging the workers to the same pathogen a year later. Transgenerational transfer of the queen’s pathogen experience to her workforce can hence durably reduce the disease susceptibility of the whole superorganism.

Methods
All experimental procedures are described in the main manuscript text or supplemental material. Data collectors: Barbara Casillas-PÈrez, Christopher D. Pull, Elisabeth Naderlinger

生命早期的感染可对生物体的发育与免疫功能产生持久影响。本研究证实，这一规律同样适用于处于发育阶段的“超有机体（superorganisms）”——即处于建立初期的社会性昆虫群落。我们将新近交尾的黑毛蚁（Lasius niger）蚁后暴露于低剂量病原体环境中，结果显示，其组建的群落冬季前的生长速率慢于对照组，但后续二者的群落规模最终趋于一致。无论是否经历病原体暴露，当蛹与工蚁的比例较低时，蚁后的越冬存活率均有所提升。蚁后在工蚁诞生前培育的蛹数量越少，其体内的病原体载量越低，这表明高强度的育幼行为会干扰蚁后免疫系统抑制病原体增殖的能力。生命早期的病原体暴露还可提升工蚁后代的免疫能力，我们在一年后用相同病原体对工蚁进行攻毒试验，证实了这一点。由此可见，蚁后将其病原体暴露经历跨代传递给工蚁种群，可持久降低整个超有机体的疾病易感性。

方法
所有实验步骤均详述于正论文文本或补充材料中。数据采集人员：Barbara Casillas-PÈrez, Christopher D. Pull, Elisabeth Naderlinger