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”).
Funding for this project was obtained by the German Research Foundation DFG (http://www.dfg.de/en/index.jsp) as an Individual Research Grant (CR118/2-1 to SC) and the European Research Council (http://erc.europa.eu/) in form of two ERC Starting Grants (ERC-2009-StG240371-SocialVaccines to SC and ERC-2010-StG259294-LatentCauses to FJT). In addition, the Junge Akademie (Young Academy of the Berlin-Brandenburg Academy of Sciences and Humanities and the National Academy of Sciences Leopoldina (http://www.diejungeakademie.de/english/index.html) funded this joint Antnet project of SC and FJT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Konrad M, Vyleta M, Theis F, et al. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biology. 2012;10(4). doi:10.1371/journal.pbio.1001300
Konrad, M., Vyleta, M., Theis, F., Stock, M., Tragust, S., Klatt, M., … Cremer, S. (2012). Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biology, 10(4). https://doi.org/10.1371/journal.pbio.1001300
Konrad, Matthias, Meghan Vyleta, Fabian Theis, Miriam Stock, Simon Tragust, Martina Klatt, Verena Drescher, Carsten Marr, Line V Ugelvig, and Sylvia Cremer. “Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies.” PLoS Biology 10, no. 4 (2012). https://doi.org/10.1371/journal.pbio.1001300.
M. Konrad et al., “Social transfer of pathogenic fungus promotes active immunisation in ant colonies,” PLoS Biology, vol. 10, no. 4, 2012.
Konrad M, Vyleta M, Theis F, Stock M, Tragust S, Klatt M, Drescher V, Marr C, Ugelvig LV, Cremer S. 2012. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biology. 10(4), e1001300.
Konrad, Matthias, et al. “Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies.” PLoS Biology, vol. 10, no. 4, e1001300, Public Library of Science, 2012, doi:10.1371/journal.pbio.1001300.