Data from: Social transfer of pathogenic fungus promotes active immunisation in ant colonies

Due to the omnipresent risk of epidemics, insect societies have evolved sophisticated disease defences at the individual and colony level. An intriguing yet little understood phenomenon is that social contact to pathogen-exposed individuals reduces susceptibility of previously naive nestmates to this pathogen. We tested whether such social immunisation in Lasius ants against the entomopathogenic fungus Metarhizium anisopliae is based on active upregulation of the immune system of nestmates following contact to an infectious individual or passive protection via transfer of immune effectors among group members—that is, active versus passive immunisation. We found no evidence for involvement of passive immunisation via transfer of antimicrobials among colony members. Instead, intensive allogrooming behaviour between naive and pathogen-exposed ants before fungal conidia firmly attached to their cuticle suggested passage of the pathogen from the exposed individuals to their nestmates. By tracing fluorescence-labelled conidia we indeed detected frequent pathogen transfer to the nestmates, where they caused low-level infections as revealed by growth of small numbers of fungal colony forming units from their dissected body content. These infections rarely led to death, but instead promoted an enhanced ability to inhibit fungal growth and an active upregulation of immune genes involved in antifungal defences (defensin and prophenoloxidase, PPO). Contrarily, there was no upregulation of the gene cathepsin L, which is associated with antibacterial and antiviral defences, and we found no increased antibacterial activity of nestmates of fungus-exposed ants. This indicates that social immunisation after fungal exposure is specific, similar to recent findings for individual-level immune priming in invertebrates. Epidemiological modeling further suggests that active social immunisation is adaptive, as it leads to faster elimination of the disease and lower death rates than passive immunisation. Interestingly, humans have also utilised the protective effect of low-level infections to fight smallpox by intentional transfer of low pathogen doses (“variolation” or “inoculation”).鉴于流行病风险无处不在，昆虫社会已演化出个体与群体层面的复杂疾病防御机制。其中一个引人关注却尚未得到充分阐释的现象是：与暴露于病原体的个体进行社交接触，可降低此前未接触过该病原体的巢伴对该病原体的易感性。本研究针对毛蚁属（Lasius）蚂蚁在遭遇昆虫病原真菌绿僵菌（Metarhizium anisopliae）时的这类社会免疫行为展开检验，以明确其机制究竟是接触感染个体后巢伴免疫系统的主动上调，还是群体成员间传递免疫效应因子所介导的被动保护——即主动免疫与被动免疫的区别。研究未发现群体成员间通过传递抗菌物质实现被动免疫的相关证据。与之相反，在真菌分生孢子牢固附着于体壁前，未接触病原体的蚂蚁与暴露个体间频繁开展的异体理毛行为，提示病原体可从暴露个体传递至巢伴。通过追踪荧光标记的分生孢子，我们确实观测到病原体频繁转移至巢伴体内；对巢伴躯体解剖后的组织进行培养，可获得少量真菌菌落形成单位，这证实其体内仅存在低水平感染。这类感染极少引发宿主死亡，反而可提升宿主抑制真菌生长的能力，并使抗真菌防御相关的免疫基因（防御素（defensin）与酚氧化酶原（prophenoloxidase, PPO））出现主动上调。与之相反，与抗菌及抗病毒防御相关的组织蛋白酶L（cathepsin L）基因并未出现上调，且暴露于真菌的蚂蚁的巢伴并未表现出抗菌活性提升。这表明真菌暴露后的社会免疫具有特异性，这与无脊椎动物个体水平免疫致敏的近期研究结果相符。流行病学建模进一步证实，主动社会免疫具有适应性：相较于被动免疫，主动社会免疫可更快实现疾病清除，并降低群体死亡率。值得注意的是，人类也曾利用低水平感染的保护效应，通过有意传递低剂量病原体来对抗天花，即"人痘接种（variolation）"或"接种（inoculation）"。