[{"oa_version":"Submitted Version","title":"Opposing effects of allogrooming on disease transmission in ant societies","author":[{"last_name":"Theis","full_name":"Theis, Fabian","first_name":"Fabian"},{"first_name":"Line V","orcid":"0000-0003-1832-8883","last_name":"Ugelvig","full_name":"Ugelvig, Line V","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Carsten","full_name":"Marr, Carsten","last_name":"Marr"},{"full_name":"Cremer, Sylvia","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","orcid":"0000-0002-2193-3868","first_name":"Sylvia"}],"day":"26","scopus_import":"1","article_type":"original","date_created":"2018-12-11T11:54:15Z","volume":370,"intvolume":"       370","abstract":[{"lang":"eng","text":"To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour—either performed towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host–pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host–pathogen systems."}],"publication_status":"published","publication_identifier":{"issn":["0962-8436"],"eissn":["1471-2970"]},"month":"05","department":[{"_id":"SyCr"}],"language":[{"iso":"eng"}],"oa":1,"user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","issue":"1669","citation":{"ista":"Theis F, Ugelvig LV, Marr C, Cremer S. 2015. Opposing effects of allogrooming on disease transmission in ant societies. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 370(1669).","chicago":"Theis, Fabian, Line V Ugelvig, Carsten Marr, and Sylvia Cremer. “Opposing Effects of Allogrooming on Disease Transmission in Ant Societies.” <i>Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences</i>. Royal Society, The, 2015. <a href=\"https://doi.org/10.1098/rstb.2014.0108\">https://doi.org/10.1098/rstb.2014.0108</a>.","apa":"Theis, F., Ugelvig, L. V., Marr, C., &#38; Cremer, S. (2015). Opposing effects of allogrooming on disease transmission in ant societies. <i>Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences</i>. Royal Society, The. <a href=\"https://doi.org/10.1098/rstb.2014.0108\">https://doi.org/10.1098/rstb.2014.0108</a>","mla":"Theis, Fabian, et al. “Opposing Effects of Allogrooming on Disease Transmission in Ant Societies.” <i>Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences</i>, vol. 370, no. 1669, Royal Society, The, 2015, doi:<a href=\"https://doi.org/10.1098/rstb.2014.0108\">10.1098/rstb.2014.0108</a>.","ama":"Theis F, Ugelvig LV, Marr C, Cremer S. Opposing effects of allogrooming on disease transmission in ant societies. <i>Philosophical Transactions of the Royal Society of London Series B, Biological Sciences</i>. 2015;370(1669). doi:<a href=\"https://doi.org/10.1098/rstb.2014.0108\">10.1098/rstb.2014.0108</a>","ieee":"F. Theis, L. V. Ugelvig, C. Marr, and S. Cremer, “Opposing effects of allogrooming on disease transmission in ant societies,” <i>Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences</i>, vol. 370, no. 1669. Royal Society, The, 2015.","short":"F. Theis, L.V. Ugelvig, C. Marr, S. Cremer, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 370 (2015)."},"publisher":"Royal Society, The","doi":"10.1098/rstb.2014.0108","article_processing_charge":"No","type":"journal_article","date_updated":"2023-02-23T14:06:12Z","_id":"1830","quality_controlled":"1","main_file_link":[{"open_access":"1","url":"http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4410374/"}],"external_id":{"pmid":["25870394"]},"related_material":{"record":[{"relation":"research_data","status":"public","id":"9721"}]},"year":"2015","publist_id":"5273","project":[{"_id":"25DC711C-B435-11E9-9278-68D0E5697425","grant_number":"243071","name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects","call_identifier":"FP7"},{"_id":"25DDF0F0-B435-11E9-9278-68D0E5697425","name":"Pathogen Detectors Collective disease defence and pathogen detection abilities in ant societies: a chemo-neuro-immunological approach","grant_number":"302004","call_identifier":"FP7"},{"name":"Antnet","_id":"25E0E184-B435-11E9-9278-68D0E5697425"},{"_id":"25E24DB2-B435-11E9-9278-68D0E5697425","name":"Fellowship of Wissenschaftskolleg zu Berlin"}],"status":"public","publication":"Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences","acknowledgement":"We thank Meghan L. Vyleta for the genetical fungal strain characterization and Eva Sixt for ant drawings, Matthias Konrad for discussion and Christopher D. Pull, Barbara Casillas-Peréz, Sebastian Novak, as well as three anonymous reviewers and the theme issue editors Peter Kappeler and Charlie Nunn for valuable comments on the manuscript.","date_published":"2015-05-26T00:00:00Z","pmid":1,"ec_funded":1},{"department":[{"_id":"SyCr"}],"article_number":"e1001300","file":[{"file_id":"4689","date_created":"2018-12-12T10:08:28Z","file_size":674228,"creator":"system","date_updated":"2020-07-14T12:46:04Z","relation":"main_file","checksum":"4ebacefd9fbab5c68adf829124115fd1","file_name":"IST-2012-96-v1+1_journal.pbio.1001300.pdf","content_type":"application/pdf","access_level":"open_access"}],"month":"04","citation":{"short":"M. Konrad, M. Vyleta, F. Theis, M. Stock, S. Tragust, M. Klatt, V. Drescher, C. Marr, L.V. Ugelvig, S. Cremer, PLoS Biology 10 (2012).","ieee":"M. Konrad <i>et al.</i>, “Social transfer of pathogenic fungus promotes active immunisation in ant colonies,” <i>PLoS Biology</i>, vol. 10, no. 4. Public Library of Science, 2012.","ama":"Konrad M, Vyleta M, Theis F, et al. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. <i>PLoS Biology</i>. 2012;10(4). doi:<a href=\"https://doi.org/10.1371/journal.pbio.1001300\">10.1371/journal.pbio.1001300</a>","mla":"Konrad, Matthias, et al. “Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies.” <i>PLoS Biology</i>, vol. 10, no. 4, e1001300, Public Library of Science, 2012, doi:<a href=\"https://doi.org/10.1371/journal.pbio.1001300\">10.1371/journal.pbio.1001300</a>.","apa":"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. <i>PLoS Biology</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pbio.1001300\">https://doi.org/10.1371/journal.pbio.1001300</a>","chicago":"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.” <i>PLoS Biology</i>. Public Library of Science, 2012. <a href=\"https://doi.org/10.1371/journal.pbio.1001300\">https://doi.org/10.1371/journal.pbio.1001300</a>.","ista":"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."},"issue":"4","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"pubrep_id":"96","language":[{"iso":"eng"}],"volume":10,"date_created":"2018-12-11T12:02:13Z","scopus_import":1,"day":"03","author":[{"id":"46528076-F248-11E8-B48F-1D18A9856A87","full_name":"Konrad, Matthias","last_name":"Konrad","first_name":"Matthias"},{"first_name":"Meghan","full_name":"Vyleta, Meghan","id":"418901AA-F248-11E8-B48F-1D18A9856A87","last_name":"Vyleta"},{"first_name":"Fabian","last_name":"Theis","full_name":"Theis, Fabian"},{"last_name":"Stock","id":"42462816-F248-11E8-B48F-1D18A9856A87","full_name":"Stock, Miriam","first_name":"Miriam"},{"first_name":"Simon","full_name":"Tragust, Simon","id":"35A7A418-F248-11E8-B48F-1D18A9856A87","last_name":"Tragust"},{"last_name":"Klatt","full_name":"Klatt, Martina","id":"E60F29C6-E9AE-11E9-AF6E-D190C7302F38","first_name":"Martina"},{"full_name":"Drescher, Verena","last_name":"Drescher","first_name":"Verena"},{"full_name":"Marr, Carsten","last_name":"Marr","first_name":"Carsten"},{"full_name":"Ugelvig, Line V","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87","last_name":"Ugelvig","first_name":"Line V","orcid":"0000-0003-1832-8883"},{"orcid":"0000-0002-2193-3868","first_name":"Sylvia","full_name":"Cremer, Sylvia","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer"}],"oa_version":"Published Version","title":"Social transfer of pathogenic fungus promotes active immunisation in ant colonies","file_date_updated":"2020-07-14T12:46:04Z","publication_status":"published","has_accepted_license":"1","intvolume":"        10","tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"abstract":[{"lang":"eng","text":"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”)."}],"publist_id":"3434","year":"2012","related_material":{"record":[{"relation":"research_data","status":"public","id":"9755"}]},"ec_funded":1,"acknowledgement":"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/i​ndex.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.","date_published":"2012-04-03T00:00:00Z","publication":"PLoS Biology","status":"public","project":[{"_id":"25DAF0B2-B435-11E9-9278-68D0E5697425","name":"Host-Parasite Coevolution","grant_number":"CR-118/3-1"},{"grant_number":"243071","name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects","call_identifier":"FP7","_id":"25DC711C-B435-11E9-9278-68D0E5697425"},{"name":"Antnet","_id":"25E0E184-B435-11E9-9278-68D0E5697425"}],"_id":"3242","date_updated":"2023-02-23T14:07:11Z","type":"journal_article","doi":"10.1371/journal.pbio.1001300","publisher":"Public Library of Science","quality_controlled":"1","ddc":["570","579"]}]