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精密疾病防御机制。但有一个引人关注却鲜少被阐明的现象：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的感染易感性。我们以毛蚁属（Lasius）蚂蚁为研究对象，探究其针对虫生真菌绿僵菌（Metarhizium anisopliae）的社交免疫，是否依赖于接触感染个体后巢伴免疫系统的主动上调，或是通过群体成员间传递免疫效应物实现的被动保护——即区分主动免疫与被动免疫两种模式。我们未发现群体成员间传递抗菌物质以实现被动免疫的相关证据。反之，在真菌分生孢子牢固附着于体壁之前，未接触病原体与暴露于病原体的蚂蚁之间存在频繁的互理毛行为，这提示病原体可从暴露个体传递至其巢伴。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传递至巢伴体内，这些病原体引发了低水平感染：对解剖后的蚁体内容物培养发现，仅长出少量真菌菌落形成单位（CFU）。此类感染极少导致宿主死亡，反而提升了宿主抑制真菌生长的能力，并激活了抗真菌防御相关免疫基因（防御素（defensin）与酚氧化酶原（prophenoloxidase，PPO））的表达上调。与之相反，与抗菌、抗病毒防御相关的组织蛋白酶L（cathepsin L）基因并未出现表达上调，且我们未观测到接触过真菌的蚂蚁的巢伴的抗菌活性有所提升。这表明真菌暴露后的社交免疫具有特异性，这与无脊椎动物个体层面免疫致敏的近期研究结果一致。流行病学模型进一步显示，主动社交免疫具有适应性优势：相较于被动免疫，它能更快地清除病原体，且降低群体死亡率。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（即人痘接种术（variolation）或接种（inoculation））来对抗天花。