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，昆虫社群已演化出个体与群体层面的精密疾病防御机制。一个引人关注却尚未被充分阐明的现象是：与暴露于病原体的个体发生社会接触，可降低此前未致敏巢伴对该病原体的易感性。我们以毛蚁属（Lasius）蚂蚁为研究对象，检验其针对昆虫病原真菌绿僵菌（Metarhizium anisopliae）的社会性免疫，究竟是通过接触感染个体后主动上调巢伴免疫系统实现，还是通过群体成员间传递免疫效应分子达成被动保护——即区分主动社会性免疫与被动社会性免疫。我们未发现群体成员间传递抗菌物质以介导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虫体体壁之前，未致敏蚂蚁与暴露个体间频繁的异体理毛行为，暗示病原体可从暴露个体转移至巢伴。通过追踪荧光标记的分生孢子，我们确实检测到病原体频繁转移至巢伴体内；对解剖获取的虫体内容物进行培养发现，仅形成少量真菌菌落形成单位，表明其引发了低水平感染。这类感染极少导致宿主死亡，反而能提升宿主抑制真菌生长的能力，并主动上调抗真菌防御相关的免疫基因（防御素与酚氧化酶原（PPO））的表达。与之相反，与抗菌、抗病毒防御相关的组织蛋白酶L基因并未出现表达上调，且我们未观察到暴露于真菌的蚂蚁的巢伴抗菌活性有所提升。这表明真菌暴露后的社会性免疫具有特异性，这与无脊椎动物个体层面免疫致敏的最新研究结果一致。流行病学建模进一步表明，主动社会性免疫具有适应性优势：相较于被动免疫，它能更快清除病原体，且致死率更低。值得注意的是，人类也曾利用低水平感染的保护效应，通过故意传递低剂量病原体来对抗天花，即人痘接种法（variolation）或接种（inoculation）。