[{"date_published":"2015-01-22T00:00:00Z","author":[{"last_name":"Konrad","id":"46528076-F248-11E8-B48F-1D18A9856A87","first_name":"Matthias","full_name":"Konrad, Matthias"},{"first_name":"Anna V","full_name":"Grasse, Anna V","id":"406F989C-F248-11E8-B48F-1D18A9856A87","last_name":"Grasse"},{"first_name":"Simon","full_name":"Tragust, Simon","last_name":"Tragust","id":"35A7A418-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0002-2193-3868","last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","full_name":"Cremer, Sylvia","first_name":"Sylvia"}],"oa":1,"_id":"1993","type":"journal_article","language":[{"iso":"eng"}],"doi":"10.1098/rspb.2014.1976","publisher":"The Royal Society","year":"2015","volume":282,"article_type":"original","month":"01","quality_controlled":"1","publication_identifier":{"issn":["0962-8452"],"eissn":["1471-2954"]},"publist_id":"5090","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","article_processing_charge":"No","intvolume":"       282","article_number":"20141976","date_created":"2018-12-11T11:55:06Z","pmid":1,"department":[{"_id":"SyCr"}],"acknowledgement":"Funding was obtained by the German Research Foundation (CR 118–2) and an ERC StG (243071) by the European Research Council (both to S.C.).\r\nWe thank Line V. Ugelvig for help with ant collection and statistical discussion, Xavier Espadaler for detailed information on the ant collection site, Birgit Lautenschläger for the electron microscopy images and Eva Sixt for ant drawings. We further thank Jørgen Eilenberg for the fungal strain, Meghan L. Vyleta for genetic strain characterization and immune gene primer development, Paul Schmid-Hempel for discussion, and Line V. Ugelvig, Xavier Espadaler and Christopher D. Pull for comments on the manuscript. S.C., M.K. and S.T. conceived the study; M.K. and A.V.G. performed the experiments; M.K. performed the statistical analysis; S.C. and M.K. wrote the manuscript with intense contributions of A.V.G. and S.T.; all authors approved the manuscript.","publication_status":"published","oa_version":"Submitted Version","day":"22","ec_funded":1,"abstract":[{"lang":"eng","text":"The fitness effects of symbionts on their hosts can be context-dependent, with usually benign symbionts causing detrimental effects when their hosts are stressed, or typically parasitic symbionts providing protection towards their hosts (e.g. against pathogen infection). Here, we studied the novel association between the invasive garden ant Lasius neglectus and its fungal ectosymbiont Laboulbenia formicarum for potential costs and benefits. We tested ants with different Laboulbenia levels for their survival and immunity under resource limitation and exposure to the obligate killing entomopathogen Metarhizium brunneum. While survival of L. neglectus workers under starvation was significantly decreased with increasing Laboulbenia levels, host survival under Metarhizium exposure increased with higher levels of the ectosymbiont, suggesting a symbiont-mediated anti-pathogen protection, which seems to be driven mechanistically by both improved sanitary behaviours and an upregulated immune system. Ants with high Laboulbenia levels showed significantly longer self-grooming and elevated expression of immune genes relevant for wound repair and antifungal responses (β-1,3-glucan binding protein, Prophenoloxidase), compared with ants carrying low Laboulbenia levels. This suggests that the ectosymbiont Laboulbenia formicarum weakens its ant host by either direct resource exploitation or the costs of an upregulated behavioural and immunological response, which, however, provides a prophylactic protection upon later exposure to pathogens. "}],"acknowledged_ssus":[{"_id":"EM-Fac"}],"status":"public","date_updated":"2023-02-23T14:06:41Z","publication":"Proceedings of the Royal Society of London Series B Biological Sciences","related_material":{"record":[{"status":"public","id":"9740","relation":"research_data"}]},"external_id":{"pmid":["25473011"]},"title":"Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host","main_file_link":[{"open_access":"1","url":"http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4286035/"}],"issue":"1799","scopus_import":"1","project":[{"call_identifier":"FP7","grant_number":"243071","_id":"25DC711C-B435-11E9-9278-68D0E5697425","name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects"},{"name":"Host-Parasite Coevolution","_id":"25DAF0B2-B435-11E9-9278-68D0E5697425","grant_number":"CR-118/3-1"}],"citation":{"ama":"Konrad M, Grasse AV, Tragust S, Cremer S. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. <i>Proceedings of the Royal Society of London Series B Biological Sciences</i>. 2015;282(1799). doi:<a href=\"https://doi.org/10.1098/rspb.2014.1976\">10.1098/rspb.2014.1976</a>","mla":"Konrad, Matthias, et al. “Anti-Pathogen Protection versus Survival Costs Mediated by an Ectosymbiont in an Ant Host.” <i>Proceedings of the Royal Society of London Series B Biological Sciences</i>, vol. 282, no. 1799, 20141976, The Royal Society, 2015, doi:<a href=\"https://doi.org/10.1098/rspb.2014.1976\">10.1098/rspb.2014.1976</a>.","apa":"Konrad, M., Grasse, A. V., Tragust, S., &#38; Cremer, S. (2015). Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. <i>Proceedings of the Royal Society of London Series B Biological Sciences</i>. The Royal Society. <a href=\"https://doi.org/10.1098/rspb.2014.1976\">https://doi.org/10.1098/rspb.2014.1976</a>","short":"M. Konrad, A.V. Grasse, S. Tragust, S. Cremer, Proceedings of the Royal Society of London Series B Biological Sciences 282 (2015).","ista":"Konrad M, Grasse AV, Tragust S, Cremer S. 2015. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proceedings of the Royal Society of London Series B Biological Sciences. 282(1799), 20141976.","ieee":"M. Konrad, A. V. Grasse, S. Tragust, and S. Cremer, “Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host,” <i>Proceedings of the Royal Society of London Series B Biological Sciences</i>, vol. 282, no. 1799. The Royal Society, 2015.","chicago":"Konrad, Matthias, Anna V Grasse, Simon Tragust, and Sylvia Cremer. “Anti-Pathogen Protection versus Survival Costs Mediated by an Ectosymbiont in an Ant Host.” <i>Proceedings of the Royal Society of London Series B Biological Sciences</i>. The Royal Society, 2015. <a href=\"https://doi.org/10.1098/rspb.2014.1976\">https://doi.org/10.1098/rspb.2014.1976</a>."}},{"department":[{"_id":"SyCr"}],"pmid":1,"date_created":"2018-12-11T11:52:39Z","intvolume":"        81","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publist_id":"5623","quality_controlled":"1","month":"12","volume":81,"year":"2015","publisher":"American Society for Microbiology","doi":"10.1128/AEM.02051-15","language":[{"iso":"eng"}],"type":"journal_article","_id":"1548","oa":1,"author":[{"first_name":"Barbara","full_name":"Milutinovic, Barbara","last_name":"Milutinovic","id":"2CDC32B8-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-8214-4758"},{"last_name":"Höfling","first_name":"Christina","full_name":"Höfling, Christina"},{"last_name":"Futo","full_name":"Futo, Momir","first_name":"Momir"},{"first_name":"Jörn","full_name":"Scharsack, Jörn","last_name":"Scharsack"},{"last_name":"Kurtz","first_name":"Joachim","full_name":"Kurtz, Joachim"}],"date_published":"2015-12-01T00:00:00Z","citation":{"ama":"Milutinovic B, Höfling C, Futo M, Scharsack J, Kurtz J. Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination. <i>Applied and Environmental Microbiology</i>. 2015;81(23):8135-8144. doi:<a href=\"https://doi.org/10.1128/AEM.02051-15\">10.1128/AEM.02051-15</a>","mla":"Milutinovic, Barbara, et al. “Infection of Tribolium Castaneum with Bacillus Thuringiensis: Quantification of Bacterial Replication within Cadavers, Transmission via Cannibalism, and Inhibition of Spore Germination.” <i>Applied and Environmental Microbiology</i>, vol. 81, no. 23, American Society for Microbiology, 2015, pp. 8135–44, doi:<a href=\"https://doi.org/10.1128/AEM.02051-15\">10.1128/AEM.02051-15</a>.","short":"B. Milutinovic, C. Höfling, M. Futo, J. Scharsack, J. Kurtz, Applied and Environmental Microbiology 81 (2015) 8135–8144.","apa":"Milutinovic, B., Höfling, C., Futo, M., Scharsack, J., &#38; Kurtz, J. (2015). Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination. <i>Applied and Environmental Microbiology</i>. American Society for Microbiology. <a href=\"https://doi.org/10.1128/AEM.02051-15\">https://doi.org/10.1128/AEM.02051-15</a>","ista":"Milutinovic B, Höfling C, Futo M, Scharsack J, Kurtz J. 2015. Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination. Applied and Environmental Microbiology. 81(23), 8135–8144.","ieee":"B. Milutinovic, C. Höfling, M. Futo, J. Scharsack, and J. Kurtz, “Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination,” <i>Applied and Environmental Microbiology</i>, vol. 81, no. 23. American Society for Microbiology, pp. 8135–8144, 2015.","chicago":"Milutinovic, Barbara, Christina Höfling, Momir Futo, Jörn Scharsack, and Joachim Kurtz. “Infection of Tribolium Castaneum with Bacillus Thuringiensis: Quantification of Bacterial Replication within Cadavers, Transmission via Cannibalism, and Inhibition of Spore Germination.” <i>Applied and Environmental Microbiology</i>. American Society for Microbiology, 2015. <a href=\"https://doi.org/10.1128/AEM.02051-15\">https://doi.org/10.1128/AEM.02051-15</a>."},"scopus_import":1,"issue":"23","main_file_link":[{"url":"http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4651099/","open_access":"1"}],"title":"Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination","external_id":{"pmid":["26386058"]},"publication":"Applied and Environmental Microbiology","date_updated":"2021-01-12T06:51:31Z","status":"public","abstract":[{"text":"Reproduction within a host and transmission to the next host are crucial for the virulence and fitness of pathogens. Nevertheless, basic knowledge about such parameters is often missing from the literature, even for well-studied bacteria, such as Bacillus thuringiensis, an endospore-forming insect pathogen, which infects its hosts via the oral route. To characterize bacterial replication success, we made use of an experimental oral infection system for the red flour beetle Tribolium castaneum and developed a flow cytometric assay for the quantification of both spore ingestion by the individual beetle larvae and the resulting spore load after bacterial replication and resporulation within cadavers. On average, spore numbers increased 460-fold, showing that Bacillus thuringiensis grows and replicates successfully in insect cadavers. By inoculating cadaver-derived spores and spores from bacterial stock cultures into nutrient medium, we next investigated outgrowth characteristics of vegetative cells and found that cadaver- derived bacteria showed reduced growth compared to bacteria from the stock cultures. Interestingly, this reduced growth was a consequence of inhibited spore germination, probably originating from the host and resulting in reduced host mortality in subsequent infections by cadaver-derived spores. Nevertheless, we further showed that Bacillus thuringiensis transmission was possible via larval cannibalism when no other food was offered. These results contribute to our understanding of the ecology of Bacillus thuringiensis as an insect pathogen.","lang":"eng"}],"day":"01","oa_version":"Submitted Version","publication_status":"published","page":"8135 - 8144"},{"_id":"1551","oa":1,"author":[{"last_name":"El Masri","id":"349A6E66-F248-11E8-B48F-1D18A9856A87","first_name":"Leila","full_name":"El Masri, Leila"},{"full_name":"Branca, Antoine","first_name":"Antoine","last_name":"Branca"},{"last_name":"Sheppard","full_name":"Sheppard, Anna","first_name":"Anna"},{"first_name":"Andrei","full_name":"Papkou, Andrei","last_name":"Papkou"},{"last_name":"Laehnemann","full_name":"Laehnemann, David","first_name":"David"},{"last_name":"Guenther","first_name":"Patrick","full_name":"Guenther, Patrick"},{"full_name":"Prahl, Swantje","first_name":"Swantje","last_name":"Prahl"},{"first_name":"Manja","full_name":"Saebelfeld, Manja","last_name":"Saebelfeld"},{"last_name":"Hollensteiner","first_name":"Jacqueline","full_name":"Hollensteiner, Jacqueline"},{"last_name":"Liesegang","full_name":"Liesegang, Heiko","first_name":"Heiko"},{"last_name":"Brzuszkiewicz","first_name":"Elzbieta","full_name":"Brzuszkiewicz, Elzbieta"},{"full_name":"Daniel, Rolf","first_name":"Rolf","last_name":"Daniel"},{"first_name":"Nico","full_name":"Michiels, Nico","last_name":"Michiels"},{"last_name":"Schulte","first_name":"Rebecca","full_name":"Schulte, Rebecca"},{"full_name":"Kurtz, Joachim","first_name":"Joachim","last_name":"Kurtz"},{"last_name":"Rosenstiel","full_name":"Rosenstiel, Philip","first_name":"Philip"},{"full_name":"Telschow, Arndt","first_name":"Arndt","last_name":"Telschow"},{"first_name":"Erich","full_name":"Bornberg Bauer, Erich","last_name":"Bornberg Bauer"},{"full_name":"Schulenburg, Hinrich","first_name":"Hinrich","last_name":"Schulenburg"}],"date_published":"2015-06-04T00:00:00Z","year":"2015","publisher":"Public Library of Science","doi":"10.1371/journal.pbio.1002169","language":[{"iso":"eng"}],"type":"journal_article","publist_id":"5620","quality_controlled":"1","month":"06","volume":13,"acknowledgement":"We are very grateful for funding from the German Science Foundation (DFG) to HS (SCHU 1415/8, SCHU 1415/9), PR (RO 2994/3), EBB (BO 2544/7), HL (LI 1690/2), AT (TE 976/2), RDS (SCHU 2522/1), JK (KU 1929/4); from the Kiel Excellence Cluster Inflammation at Interfaces to HS and PR; and from the ISTFELLOW program (Co-fund Marie Curie Actions of the European Commission) to LM.","department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:52:40Z","intvolume":"        13","file_date_updated":"2020-07-14T12:45:02Z","user_id":"3E5EF7F0-F248-11E8-B48F-1D18A9856A87","ddc":["570"],"abstract":[{"text":"Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen–host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins.We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogen's genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host–pathogen interaction system.","lang":"eng"}],"ec_funded":1,"day":"04","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"page":"1 - 30","oa_version":"Published Version","publication_status":"published","date_updated":"2021-01-12T06:51:33Z","license":"https://creativecommons.org/licenses/by/4.0/","status":"public","file":[{"date_updated":"2020-07-14T12:45:02Z","date_created":"2018-12-12T10:14:13Z","checksum":"30dee7a2c11ed09f2f5634655c0146f8","file_id":"5063","file_size":3468956,"file_name":"IST-2016-481-v1+1_journal.pbio.1002169.pdf","relation":"main_file","content_type":"application/pdf","access_level":"open_access","creator":"system"}],"title":"Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes","publication":"PLoS Biology","citation":{"ama":"El Masri L, Branca A, Sheppard A, et al. Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes. <i>PLoS Biology</i>. 2015;13(6):1-30. doi:<a href=\"https://doi.org/10.1371/journal.pbio.1002169\">10.1371/journal.pbio.1002169</a>","apa":"El Masri, L., Branca, A., Sheppard, A., Papkou, A., Laehnemann, D., Guenther, P., … Schulenburg, H. (2015). Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes. <i>PLoS Biology</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pbio.1002169\">https://doi.org/10.1371/journal.pbio.1002169</a>","mla":"El Masri, Leila, et al. “Host–Pathogen Coevolution: The Selective Advantage of Bacillus Thuringiensis Virulence and Its Cry Toxin Genes.” <i>PLoS Biology</i>, vol. 13, no. 6, Public Library of Science, 2015, pp. 1–30, doi:<a href=\"https://doi.org/10.1371/journal.pbio.1002169\">10.1371/journal.pbio.1002169</a>.","ista":"El Masri L, Branca A, Sheppard A, Papkou A, Laehnemann D, Guenther P, Prahl S, Saebelfeld M, Hollensteiner J, Liesegang H, Brzuszkiewicz E, Daniel R, Michiels N, Schulte R, Kurtz J, Rosenstiel P, Telschow A, Bornberg Bauer E, Schulenburg H. 2015. Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes. PLoS Biology. 13(6), 1–30.","short":"L. El Masri, A. Branca, A. Sheppard, A. Papkou, D. Laehnemann, P. Guenther, S. Prahl, M. Saebelfeld, J. Hollensteiner, H. Liesegang, E. Brzuszkiewicz, R. Daniel, N. Michiels, R. Schulte, J. Kurtz, P. Rosenstiel, A. Telschow, E. Bornberg Bauer, H. Schulenburg, PLoS Biology 13 (2015) 1–30.","ieee":"L. El Masri <i>et al.</i>, “Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes,” <i>PLoS Biology</i>, vol. 13, no. 6. Public Library of Science, pp. 1–30, 2015.","chicago":"El Masri, Leila, Antoine Branca, Anna Sheppard, Andrei Papkou, David Laehnemann, Patrick Guenther, Swantje Prahl, et al. “Host–Pathogen Coevolution: The Selective Advantage of Bacillus Thuringiensis Virulence and Its Cry Toxin Genes.” <i>PLoS Biology</i>. Public Library of Science, 2015. <a href=\"https://doi.org/10.1371/journal.pbio.1002169\">https://doi.org/10.1371/journal.pbio.1002169</a>."},"project":[{"grant_number":"291734","call_identifier":"FP7","_id":"25681D80-B435-11E9-9278-68D0E5697425","name":"International IST Postdoc Fellowship Programme"}],"pubrep_id":"481","has_accepted_license":"1","scopus_import":1,"issue":"6"},{"date_created":"2021-07-26T09:38:36Z","department":[{"_id":"SyCr"}],"citation":{"mla":"Theis, Fabian, et al. <i>Data from: Opposing Effects of Allogrooming on Disease Transmission in Ant Societies</i>. Dryad, 2015, doi:<a href=\"https://doi.org/10.5061/dryad.dj2bf\">10.5061/dryad.dj2bf</a>.","ista":"Theis F, Ugelvig LV, Marr C, Cremer S. 2015. Data from: Opposing effects of allogrooming on disease transmission in ant societies, Dryad, <a href=\"https://doi.org/10.5061/dryad.dj2bf\">10.5061/dryad.dj2bf</a>.","apa":"Theis, F., Ugelvig, L. V., Marr, C., &#38; Cremer, S. (2015). Data from: Opposing effects of allogrooming on disease transmission in ant societies. Dryad. <a href=\"https://doi.org/10.5061/dryad.dj2bf\">https://doi.org/10.5061/dryad.dj2bf</a>","short":"F. Theis, L.V. Ugelvig, C. Marr, S. Cremer, (2015).","ama":"Theis F, Ugelvig LV, Marr C, Cremer S. Data from: Opposing effects of allogrooming on disease transmission in ant societies. 2015. doi:<a href=\"https://doi.org/10.5061/dryad.dj2bf\">10.5061/dryad.dj2bf</a>","chicago":"Theis, Fabian, Line V Ugelvig, Carsten Marr, and Sylvia Cremer. “Data from: Opposing Effects of Allogrooming on Disease Transmission in Ant Societies.” Dryad, 2015. <a href=\"https://doi.org/10.5061/dryad.dj2bf\">https://doi.org/10.5061/dryad.dj2bf</a>.","ieee":"F. Theis, L. V. Ugelvig, C. Marr, and S. Cremer, “Data from: Opposing effects of allogrooming on disease transmission in ant societies.” Dryad, 2015."},"article_processing_charge":"No","user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","month":"12","main_file_link":[{"open_access":"1","url":"https://doi.org/10.5061/dryad.dj2bf"}],"related_material":{"record":[{"relation":"used_in_publication","id":"1830","status":"public"}]},"title":"Data from: Opposing effects of allogrooming on disease transmission in ant societies","doi":"10.5061/dryad.dj2bf","publisher":"Dryad","date_updated":"2023-02-23T10:16:22Z","year":"2015","status":"public","type":"research_data_reference","author":[{"full_name":"Theis, Fabian","first_name":"Fabian","last_name":"Theis"},{"id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87","last_name":"Ugelvig","orcid":"0000-0003-1832-8883","full_name":"Ugelvig, Line V","first_name":"Line V"},{"first_name":"Carsten","full_name":"Marr, Carsten","last_name":"Marr"},{"orcid":"0000-0002-2193-3868","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","first_name":"Sylvia","full_name":"Cremer, Sylvia"}],"oa":1,"_id":"9721","date_published":"2015-12-29T00:00:00Z","oa_version":"Published Version","day":"29","abstract":[{"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.","lang":"eng"}]},{"user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","article_processing_charge":"No","date_created":"2021-07-28T08:52:53Z","department":[{"_id":"SyCr"}],"citation":{"ista":"Westhus C, Ugelvig LV, Tourdot E, Heinze J, Doums C, Cremer S. 2015. Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant, Dryad, <a href=\"https://doi.org/10.5061/dryad.7kc79\">10.5061/dryad.7kc79</a>.","short":"C. Westhus, L.V. Ugelvig, E. Tourdot, J. Heinze, C. Doums, S. Cremer, (2015).","mla":"Westhus, Claudia, et al. <i>Data from: Increased Grooming after Repeated Brood Care Provides Sanitary Benefits in a Clonal Ant</i>. Dryad, 2015, doi:<a href=\"https://doi.org/10.5061/dryad.7kc79\">10.5061/dryad.7kc79</a>.","apa":"Westhus, C., Ugelvig, L. V., Tourdot, E., Heinze, J., Doums, C., &#38; Cremer, S. (2015). Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. Dryad. <a href=\"https://doi.org/10.5061/dryad.7kc79\">https://doi.org/10.5061/dryad.7kc79</a>","ama":"Westhus C, Ugelvig LV, Tourdot E, Heinze J, Doums C, Cremer S. Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. 2015. doi:<a href=\"https://doi.org/10.5061/dryad.7kc79\">10.5061/dryad.7kc79</a>","chicago":"Westhus, Claudia, Line V Ugelvig, Edouard Tourdot, Jürgen Heinze, Claudie Doums, and Sylvia Cremer. “Data from: Increased Grooming after Repeated Brood Care Provides Sanitary Benefits in a Clonal Ant.” Dryad, 2015. <a href=\"https://doi.org/10.5061/dryad.7kc79\">https://doi.org/10.5061/dryad.7kc79</a>.","ieee":"C. Westhus, L. V. Ugelvig, E. Tourdot, J. Heinze, C. Doums, and S. Cremer, “Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant.” Dryad, 2015."},"title":"Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant","related_material":{"record":[{"status":"public","id":"2161","relation":"used_in_publication"}]},"month":"07","main_file_link":[{"open_access":"1","url":"https://doi.org/10.5061/dryad.7kc79"}],"status":"public","type":"research_data_reference","doi":"10.5061/dryad.7kc79","year":"2015","date_updated":"2023-02-23T10:30:52Z","publisher":"Dryad","day":"09","date_published":"2015-07-09T00:00:00Z","oa_version":"Published Version","abstract":[{"lang":"eng","text":"Repeated pathogen exposure is a common threat in colonies of social insects, posing selection pressures on colony members to respond with improved disease-defense performance. We here tested whether experience gained by repeated tending of low-level fungus-exposed (Metarhizium robertsii) larvae may alter the performance of sanitary brood care in the clonal ant, Platythyrea punctata. We trained ants individually over nine consecutive trials to either sham-treated or fungus-exposed larvae. We then compared the larval grooming behavior of naive and trained ants and measured how effectively they removed infectious fungal conidiospores from the fungus-exposed larvae. We found that the ants changed the duration of larval grooming in response to both, larval treatment and their level of experience: (1) sham-treated larvae received longer grooming than the fungus-exposed larvae and (2) trained ants performed less self-grooming but longer larval grooming than naive ants, which was true for both, ants trained to fungus-exposed and also to sham-treated larvae. Ants that groomed the fungus-exposed larvae for longer periods removed a higher number of fungal conidiospores from the surface of the fungus-exposed larvae. As experienced ants performed longer larval grooming, they were more effective in fungal removal, thus making them better caretakers under pathogen attack of the colony. By studying this clonal ant, we can thus conclude that even in the absence of genetic variation between colony members, differences in experience levels of brood care may affect performance of sanitary brood care in social insects."}],"author":[{"last_name":"Westhus","full_name":"Westhus, Claudia","first_name":"Claudia"},{"first_name":"Line V","full_name":"Ugelvig, Line V","orcid":"0000-0003-1832-8883","last_name":"Ugelvig","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Tourdot, Edouard","first_name":"Edouard","last_name":"Tourdot"},{"full_name":"Heinze, Jürgen","first_name":"Jürgen","last_name":"Heinze"},{"last_name":"Doums","full_name":"Doums, Claudie","first_name":"Claudie"},{"id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","orcid":"0000-0002-2193-3868","first_name":"Sylvia","full_name":"Cremer, Sylvia"}],"_id":"9742","oa":1},{"quality_controlled":"1","publist_id":"5208","main_file_link":[{"open_access":"1","url":"https://www.dzg-ev.de/wp-content/uploads/2019/05/zoologie2014.pdf"}],"month":"01","article_type":"original","title":"Gemeinsame Krankheitsabwehr in Ameisengesellschaften","publication":"Zoologie","citation":{"ama":"Cremer S. Gemeinsame Krankheitsabwehr in Ameisengesellschaften. <i>Zoologie</i>. 2014:23-30.","apa":"Cremer, S. (2014). Gemeinsame Krankheitsabwehr in Ameisengesellschaften. <i>Zoologie</i>. Deutsche Zoologische Gesellschaft.","ista":"Cremer S. 2014. Gemeinsame Krankheitsabwehr in Ameisengesellschaften. Zoologie., 23–30.","short":"S. Cremer, Zoologie (2014) 23–30.","mla":"Cremer, Sylvia. “Gemeinsame Krankheitsabwehr in Ameisengesellschaften.” <i>Zoologie</i>, Deutsche Zoologische Gesellschaft, 2014, pp. 23–30.","ieee":"S. Cremer, “Gemeinsame Krankheitsabwehr in Ameisengesellschaften,” <i>Zoologie</i>. Deutsche Zoologische Gesellschaft, pp. 23–30, 2014.","chicago":"Cremer, Sylvia. “Gemeinsame Krankheitsabwehr in Ameisengesellschaften.” <i>Zoologie</i>. Deutsche Zoologische Gesellschaft, 2014."},"department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:54:33Z","article_processing_charge":"No","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"_id":"1887","author":[{"orcid":"0000-0002-2193-3868","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","full_name":"Cremer, Sylvia","first_name":"Sylvia"}],"page":"23 - 30","date_published":"2014-01-01T00:00:00Z","oa_version":"Published Version","publication_status":"published","day":"01","date_updated":"2023-10-17T07:54:57Z","publisher":"Deutsche Zoologische Gesellschaft","year":"2014","language":[{"iso":"eng"}],"type":"journal_article","status":"public"},{"publication":"Soziale Insekten in einer sich wandelnden Welt","title":"Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt  Bayerische Akademie der Wissenschaften","volume":43,"month":"01","publication_identifier":{"issn":["2366-2875"]},"publist_id":"5207","quality_controlled":"1","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","article_processing_charge":"No","intvolume":"        43","alternative_title":["Rundgespräche der Kommission für Ökologie"],"date_created":"2018-12-11T11:54:33Z","department":[{"_id":"SyCr"}],"citation":{"ieee":"S. Cremer, “Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt  Bayerische Akademie der Wissenschaften,” in <i>Soziale Insekten in einer sich wandelnden Welt</i>, vol. 43, Verlag Dr. Friedrich Pfeil, 2014, pp. 65–72.","chicago":"Cremer, Sylvia. “Soziale Immunität: Wie Sich Der Staat Gegen Pathogene Wehrt  Bayerische Akademie Der Wissenschaften.” In <i>Soziale Insekten in Einer Sich Wandelnden Welt</i>, 43:65–72. Verlag Dr. Friedrich Pfeil, 2014.","ama":"Cremer S. Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt  Bayerische Akademie der Wissenschaften. In: <i>Soziale Insekten in Einer Sich Wandelnden Welt</i>. Vol 43. Verlag Dr. Friedrich Pfeil; 2014:65-72.","apa":"Cremer, S. (2014). Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt  Bayerische Akademie der Wissenschaften. In <i>Soziale Insekten in einer sich wandelnden Welt</i> (Vol. 43, pp. 65–72). Verlag Dr. Friedrich Pfeil.","mla":"Cremer, Sylvia. “Soziale Immunität: Wie Sich Der Staat Gegen Pathogene Wehrt  Bayerische Akademie Der Wissenschaften.” <i>Soziale Insekten in Einer Sich Wandelnden Welt</i>, vol. 43, Verlag Dr. Friedrich Pfeil, 2014, pp. 65–72.","short":"S. Cremer, in:, Soziale Insekten in Einer Sich Wandelnden Welt, Verlag Dr. Friedrich Pfeil, 2014, pp. 65–72.","ista":"Cremer S. 2014.Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt  Bayerische Akademie der Wissenschaften. In: Soziale Insekten in einer sich wandelnden Welt. Rundgespräche der Kommission für Ökologie, vol. 43, 65–72."},"day":"01","publication_status":"published","page":"65 - 72","oa_version":"None","date_published":"2014-01-01T00:00:00Z","abstract":[{"lang":"ger","text":"Im Rahmen meiner Arbeit mit der kollektiven Krankheitsabwehr in Ameisengesellschaften interessiert mich vor allem, wie sich die Kolonien als Ganzes gegen Krankheiten wehren können. Warum ist dieses Thema der Krankheitsdynamik in Gruppen so wichtig? Ein Vergleich von solitär lebenden Individuen mit Individuen, die in sozialen Gruppen zusammenleben, zeigt die Kosten und die Vorteile des Gruppenlebens: Einerseits haben Individuen in sozialen Gruppen aufgrund der hohen Dichte, in der die Tiere zusammenleben, den hohen Interaktionsraten, die sie miteinander haben, und der engen Verwandtschaft, die sie verbindet, ein höheres Ansteckungsrisiko. Andererseits kann die individuelle Krankheitsabwehr durch die kollektive Abwehr in den Gruppen ergänzt werden."}],"author":[{"full_name":"Cremer, Sylvia","first_name":"Sylvia","orcid":"0000-0002-2193-3868","last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87"}],"_id":"1888","status":"public","type":"book_chapter","language":[{"iso":"eng"}],"year":"2014","date_updated":"2023-10-17T12:28:45Z","publisher":"Verlag Dr. Friedrich Pfeil"},{"abstract":[{"lang":"eng","text":"The unprecedented polymorphism in the major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection from parasites. However, do parasites also drive divergence at MHC loci between host populations, or do the effects of balancing selection maintain similarities among populations? We examined MHC variation in populations of the livebearing fish Poecilia mexicana and characterized their parasite communities. Poecilia mexicana populations in the Cueva del Azufre system are locally adapted to darkness and the presence of toxic hydrogen sulphide, representing highly divergent ecotypes or incipient species. Parasite communities differed significantly across populations, and populations with higher parasite loads had higher levels of diversity at class II MHC genes. However, despite different parasite communities, marked divergence in adaptive traits and in neutral genetic markers, we found MHC alleles to be remarkably similar among host populations. Our findings indicate that balancing selection from parasites maintains immunogenetic diversity of hosts, but this process does not promote MHC divergence in this system. On the contrary, we suggest that balancing selection on immunogenetic loci may outweigh divergent selection causing divergence, thereby hindering host divergence and speciation. Our findings support the hypothesis that balancing selection maintains MHC similarities among lineages during and after speciation (trans-species evolution)."}],"day":"12","oa_version":"None","publication_status":"published","page":"960 - 974","date_updated":"2022-06-07T09:22:20Z","status":"public","title":"Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations","external_id":{"pmid":["24725091"]},"publication":"Journal of Evolutionary Biology","citation":{"ama":"Tobler M, Plath M, Riesch R, et al. Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations. <i>Journal of Evolutionary Biology</i>. 2014;27(5):960-974. doi:<a href=\"https://doi.org/10.1111/jeb.12370\">10.1111/jeb.12370</a>","mla":"Tobler, Michael, et al. “Selection from Parasites Favours Immunogenetic Diversity but Not Divergence among Locally Adapted Host Populations.” <i>Journal of Evolutionary Biology</i>, vol. 27, no. 5, Wiley, 2014, pp. 960–74, doi:<a href=\"https://doi.org/10.1111/jeb.12370\">10.1111/jeb.12370</a>.","apa":"Tobler, M., Plath, M., Riesch, R., Schlupp, I., Grasse, A. V., Munimanda, G., … Moodley, Y. (2014). Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations. <i>Journal of Evolutionary Biology</i>. Wiley. <a href=\"https://doi.org/10.1111/jeb.12370\">https://doi.org/10.1111/jeb.12370</a>","short":"M. Tobler, M. Plath, R. Riesch, I. Schlupp, A.V. Grasse, G. Munimanda, C. Setzer, D. Penn, Y. Moodley, Journal of Evolutionary Biology 27 (2014) 960–974.","ista":"Tobler M, Plath M, Riesch R, Schlupp I, Grasse AV, Munimanda G, Setzer C, Penn D, Moodley Y. 2014. Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations. Journal of Evolutionary Biology. 27(5), 960–974.","ieee":"M. Tobler <i>et al.</i>, “Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations,” <i>Journal of Evolutionary Biology</i>, vol. 27, no. 5. Wiley, pp. 960–974, 2014.","chicago":"Tobler, Michael, Martin Plath, Rüdiger Riesch, Ingo Schlupp, Anna V Grasse, Gopi Munimanda, C Setzer, Dustin Penn, and Yoshan Moodley. “Selection from Parasites Favours Immunogenetic Diversity but Not Divergence among Locally Adapted Host Populations.” <i>Journal of Evolutionary Biology</i>. Wiley, 2014. <a href=\"https://doi.org/10.1111/jeb.12370\">https://doi.org/10.1111/jeb.12370</a>."},"scopus_import":"1","issue":"5","_id":"1905","author":[{"full_name":"Tobler, Michael","first_name":"Michael","last_name":"Tobler"},{"full_name":"Plath, Martin","first_name":"Martin","last_name":"Plath"},{"last_name":"Riesch","first_name":"Rüdiger","full_name":"Riesch, Rüdiger"},{"full_name":"Schlupp, Ingo","first_name":"Ingo","last_name":"Schlupp"},{"full_name":"Grasse, Anna V","first_name":"Anna V","last_name":"Grasse","id":"406F989C-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Gopi","full_name":"Munimanda, Gopi","last_name":"Munimanda"},{"first_name":"C","full_name":"Setzer, C","last_name":"Setzer"},{"last_name":"Penn","first_name":"Dustin","full_name":"Penn, Dustin"},{"first_name":"Yoshan","full_name":"Moodley, Yoshan","last_name":"Moodley"}],"date_published":"2014-04-12T00:00:00Z","year":"2014","publisher":"Wiley","doi":"10.1111/jeb.12370","language":[{"iso":"eng"}],"type":"journal_article","publist_id":"5190","publication_identifier":{"eissn":["1420-9101"],"issn":["1010-061X"]},"quality_controlled":"1","month":"04","article_type":"original","volume":27,"acknowledgement":"This study was funded by grants from the National Science Foundation (NSF) to MT (IOS-1121832) and IS (DEB-0743406) and from the German Science Foundation (DFG; PL 470/1-2) and ‘LOEWE − Landesoffensive zur Entwicklung wissenschaftlich-ökonomischer Exzellenz’ of Hesse's Ministry of Higher Education, Research, and the Arts, to MP.","department":[{"_id":"SyCr"}],"pmid":1,"date_created":"2018-12-11T11:54:38Z","intvolume":"        27","article_processing_charge":"No","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87"},{"status":"public","type":"journal_article","language":[{"iso":"eng"}],"doi":"10.1016/j.it.2014.08.005","date_updated":"2021-01-12T06:54:35Z","publisher":"Elsevier","year":"2014","date_published":"2014-10-01T00:00:00Z","publication_status":"published","oa_version":"None","page":"471 - 482","day":"01","abstract":[{"lang":"eng","text":"Immune systems are able to protect the body against secondary infection with the same parasite. In insect colonies, this protection is not restricted to the level of the individual organism, but also occurs at the societal level. Here, we review recent evidence for and insights into the mechanisms underlying individual and social immunisation in insects. We disentangle general immune-protective effects from specific immune memory (priming), and examine immunisation in the context of the lifetime of an individual and that of a colony, and of transgenerational immunisation that benefits offspring. When appropriate, we discuss parallels with disease defence strategies in human societies. We propose that recurrent parasitic threats have shaped the evolution of both the individual immune systems and colony-level social immunity in insects."}],"author":[{"last_name":"El Masri","id":"349A6E66-F248-11E8-B48F-1D18A9856A87","full_name":"El Masri, Leila","first_name":"Leila"},{"id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","orcid":"0000-0002-2193-3868","first_name":"Sylvia","full_name":"Cremer, Sylvia"}],"_id":"1998","issue":"10","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","scopus_import":1,"intvolume":"        35","date_created":"2018-12-11T11:55:07Z","department":[{"_id":"SyCr"}],"citation":{"apa":"El Masri, L., &#38; Cremer, S. (2014). Individual and social immunisation in insects. <i>Trends in Immunology</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.it.2014.08.005\">https://doi.org/10.1016/j.it.2014.08.005</a>","mla":"El Masri, Leila, and Sylvia Cremer. “Individual and Social Immunisation in Insects.” <i>Trends in Immunology</i>, vol. 35, no. 10, Elsevier, 2014, pp. 471–82, doi:<a href=\"https://doi.org/10.1016/j.it.2014.08.005\">10.1016/j.it.2014.08.005</a>.","short":"L. El Masri, S. Cremer, Trends in Immunology 35 (2014) 471–482.","ista":"El Masri L, Cremer S. 2014. Individual and social immunisation in insects. Trends in Immunology. 35(10), 471–482.","ama":"El Masri L, Cremer S. Individual and social immunisation in insects. <i>Trends in Immunology</i>. 2014;35(10):471-482. doi:<a href=\"https://doi.org/10.1016/j.it.2014.08.005\">10.1016/j.it.2014.08.005</a>","chicago":"El Masri, Leila, and Sylvia Cremer. “Individual and Social Immunisation in Insects.” <i>Trends in Immunology</i>. Elsevier, 2014. <a href=\"https://doi.org/10.1016/j.it.2014.08.005\">https://doi.org/10.1016/j.it.2014.08.005</a>.","ieee":"L. El Masri and S. Cremer, “Individual and social immunisation in insects,” <i>Trends in Immunology</i>, vol. 35, no. 10. Elsevier, pp. 471–482, 2014."},"acknowledgement":"This work was funded by an ERC Starting Grant by the European Research Council (to S.C.) and the ISTFELLOW program (Co-fund Marie Curie Actions of the European Commission; to L.M.).\r\nWe thank Christopher D. Pull, Sophie A.O. Armitage, Hinrich Schulenburg, Line V. Ugelvig, Matthias Konrad, Matthias Fürst, Miriam Stock, Barbara Casillas-Perez and three anonymous referees for comments on the manuscript. ","publication":"Trends in Immunology","volume":35,"title":"Individual and social immunisation in insects","month":"10","quality_controlled":"1","publist_id":"5081"},{"status":"public","date_updated":"2024-03-25T23:30:04Z","ec_funded":1,"abstract":[{"lang":"eng","text":"Selection for disease control is believed to have contributed to shape the organisation of insect societies — leading to interaction patterns that mitigate disease transmission risk within colonies, conferring them ‘organisational immunity’. Recent studies combining epidemiological models with social network analysis have identified general properties of interaction networks that may hinder propagation of infection within groups. These can be prophylactic and/or induced upon pathogen exposure. Here we review empirical evidence for these two types of organisational immunity in social insects and describe the individual-level behaviours that underlie it. We highlight areas requiring further investigation, and emphasise the need for tighter links between theory and empirical research and between individual-level and collective-level analyses."}],"oa_version":"None","publication_status":"published","page":"1 - 15","day":"01","issue":"1","scopus_import":1,"project":[{"_id":"25DC711C-B435-11E9-9278-68D0E5697425","name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects","call_identifier":"FP7","grant_number":"243071"}],"citation":{"ieee":"N. Stroeymeyt, B. E. Casillas Perez, and S. Cremer, “Organisational immunity in social insects,” <i>Current Opinion in Insect Science</i>, vol. 5, no. 1. Elsevier, pp. 1–15, 2014.","chicago":"Stroeymeyt, Nathalie, Barbara E Casillas Perez, and Sylvia Cremer. “Organisational Immunity in Social Insects.” <i>Current Opinion in Insect Science</i>. Elsevier, 2014. <a href=\"https://doi.org/10.1016/j.cois.2014.09.001\">https://doi.org/10.1016/j.cois.2014.09.001</a>.","ama":"Stroeymeyt N, Casillas Perez BE, Cremer S. Organisational immunity in social insects. <i>Current Opinion in Insect Science</i>. 2014;5(1):1-15. doi:<a href=\"https://doi.org/10.1016/j.cois.2014.09.001\">10.1016/j.cois.2014.09.001</a>","mla":"Stroeymeyt, Nathalie, et al. “Organisational Immunity in Social Insects.” <i>Current Opinion in Insect Science</i>, vol. 5, no. 1, Elsevier, 2014, pp. 1–15, doi:<a href=\"https://doi.org/10.1016/j.cois.2014.09.001\">10.1016/j.cois.2014.09.001</a>.","apa":"Stroeymeyt, N., Casillas Perez, B. E., &#38; Cremer, S. (2014). Organisational immunity in social insects. <i>Current Opinion in Insect Science</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.cois.2014.09.001\">https://doi.org/10.1016/j.cois.2014.09.001</a>","ista":"Stroeymeyt N, Casillas Perez BE, Cremer S. 2014. Organisational immunity in social insects. Current Opinion in Insect Science. 5(1), 1–15.","short":"N. Stroeymeyt, B.E. Casillas Perez, S. Cremer, Current Opinion in Insect Science 5 (2014) 1–15."},"related_material":{"record":[{"id":"6383","relation":"dissertation_contains"},{"relation":"dissertation_contains","id":"6435","status":"public"}]},"title":"Organisational immunity in social insects","publication":"Current Opinion in Insect Science","type":"journal_article","publisher":"Elsevier","year":"2014","language":[{"iso":"eng"}],"doi":"10.1016/j.cois.2014.09.001","date_published":"2014-11-01T00:00:00Z","_id":"1999","author":[{"last_name":"Stroeymeyt","full_name":"Stroeymeyt, Nathalie","first_name":"Nathalie"},{"full_name":"Casillas Perez, Barbara E","first_name":"Barbara E","last_name":"Casillas Perez","id":"351ED2AA-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2193-3868","full_name":"Cremer, Sylvia","first_name":"Sylvia"}],"intvolume":"         5","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:55:08Z","volume":5,"quality_controlled":"1","publist_id":"5080","month":"11"},{"quality_controlled":"1","publist_id":"4949","month":"08","volume":9,"department":[{"_id":"SyCr"}],"acknowledgement":"This study was funded jointly by a grant from BBSRC, Defra, NERC, the Scottish Government and the Wellcome Trust, under the Insect Pollinators Initiative (grant numbers BB/I00097/1 and BB/I000100/1). Rothamsted Research is a national institute of bioscience strategically funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC).","date_created":"2018-12-11T11:55:37Z","article_number":"e103989","intvolume":"         9","ddc":["570"],"user_id":"4435EBFC-F248-11E8-B48F-1D18A9856A87","file_date_updated":"2020-07-14T12:45:28Z","oa":1,"_id":"2086","author":[{"full_name":"Wolf, Stephan","first_name":"Stephan","last_name":"Wolf"},{"full_name":"Mcmahon, Dino","first_name":"Dino","last_name":"Mcmahon"},{"last_name":"Lim","full_name":"Lim, Ka","first_name":"Ka"},{"id":"3C7F4840-F248-11E8-B48F-1D18A9856A87","last_name":"Pull","orcid":"0000-0003-1122-3982","full_name":"Pull, Christopher","first_name":"Christopher"},{"last_name":"Clark","first_name":"Suzanne","full_name":"Clark, Suzanne"},{"first_name":"Robert","full_name":"Paxton, Robert","last_name":"Paxton"},{"full_name":"Osborne, Juliet","first_name":"Juliet","last_name":"Osborne"}],"date_published":"2014-08-06T00:00:00Z","publisher":"Public Library of Science","year":"2014","language":[{"iso":"eng"}],"doi":"10.1371/journal.pone.0103989","type":"journal_article","related_material":{"record":[{"id":"9888","status":"public","relation":"research_data"}]},"file":[{"file_name":"IST-2016-437-v1+1_journal.pone.0103989.pdf","file_size":1013386,"file_id":"5042","date_created":"2018-12-12T10:13:55Z","checksum":"2fc62c6739eada4bddf026afbae669db","date_updated":"2020-07-14T12:45:28Z","creator":"system","access_level":"open_access","content_type":"application/pdf","relation":"main_file"}],"title":"So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees","publication":"PLoS One","citation":{"mla":"Wolf, Stephan, et al. “So near and yet so Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees.” <i>PLoS One</i>, vol. 9, no. 8, e103989, Public Library of Science, 2014, doi:<a href=\"https://doi.org/10.1371/journal.pone.0103989\">10.1371/journal.pone.0103989</a>.","ista":"Wolf S, Mcmahon D, Lim K, Pull C, Clark S, Paxton R, Osborne J. 2014. So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees. PLoS One. 9(8), e103989.","short":"S. Wolf, D. Mcmahon, K. Lim, C. Pull, S. Clark, R. Paxton, J. Osborne, PLoS One 9 (2014).","apa":"Wolf, S., Mcmahon, D., Lim, K., Pull, C., Clark, S., Paxton, R., &#38; Osborne, J. (2014). So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees. <i>PLoS One</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pone.0103989\">https://doi.org/10.1371/journal.pone.0103989</a>","ama":"Wolf S, Mcmahon D, Lim K, et al. So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees. <i>PLoS One</i>. 2014;9(8). doi:<a href=\"https://doi.org/10.1371/journal.pone.0103989\">10.1371/journal.pone.0103989</a>","chicago":"Wolf, Stephan, Dino Mcmahon, Ka Lim, Christopher Pull, Suzanne Clark, Robert Paxton, and Juliet Osborne. “So near and yet so Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees.” <i>PLoS One</i>. Public Library of Science, 2014. <a href=\"https://doi.org/10.1371/journal.pone.0103989\">https://doi.org/10.1371/journal.pone.0103989</a>.","ieee":"S. Wolf <i>et al.</i>, “So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees,” <i>PLoS One</i>, vol. 9, no. 8. Public Library of Science, 2014."},"pubrep_id":"437","has_accepted_license":"1","issue":"8","scopus_import":1,"abstract":[{"text":"Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen - Nosema ceranae (Microsporidia) - on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed.","lang":"eng"}],"publication_status":"published","oa_version":"Published Version","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"day":"06","date_updated":"2023-02-23T14:11:56Z","status":"public"},{"issue":"10","scopus_import":"1","project":[{"name":"International IST Postdoc Fellowship Programme","_id":"25681D80-B435-11E9-9278-68D0E5697425","grant_number":"291734","call_identifier":"FP7"},{"_id":"25DC711C-B435-11E9-9278-68D0E5697425","name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects","call_identifier":"FP7","grant_number":"243071"},{"name":"Host-Parasite Coevolution","_id":"25DAF0B2-B435-11E9-9278-68D0E5697425","grant_number":"CR-118/3-1"}],"citation":{"ieee":"C. Westhus, L. V. Ugelvig, E. Tourdot, J. Heinze, C. Doums, and S. Cremer, “Increased grooming after repeated brood care provides sanitary benefits in a clonal ant,” <i>Behavioral Ecology and Sociobiology</i>, vol. 68, no. 10. Springer, pp. 1701–1710, 2014.","chicago":"Westhus, Claudia, Line V Ugelvig, Edouard Tourdot, Jürgen Heinze, Claudie Doums, and Sylvia Cremer. “Increased Grooming after Repeated Brood Care Provides Sanitary Benefits in a Clonal Ant.” <i>Behavioral Ecology and Sociobiology</i>. Springer, 2014. <a href=\"https://doi.org/10.1007/s00265-014-1778-8\">https://doi.org/10.1007/s00265-014-1778-8</a>.","ama":"Westhus C, Ugelvig LV, Tourdot E, Heinze J, Doums C, Cremer S. Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. <i>Behavioral Ecology and Sociobiology</i>. 2014;68(10):1701-1710. doi:<a href=\"https://doi.org/10.1007/s00265-014-1778-8\">10.1007/s00265-014-1778-8</a>","short":"C. Westhus, L.V. Ugelvig, E. Tourdot, J. Heinze, C. Doums, S. Cremer, Behavioral Ecology and Sociobiology 68 (2014) 1701–1710.","ista":"Westhus C, Ugelvig LV, Tourdot E, Heinze J, Doums C, Cremer S. 2014. Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. Behavioral Ecology and Sociobiology. 68(10), 1701–1710.","mla":"Westhus, Claudia, et al. “Increased Grooming after Repeated Brood Care Provides Sanitary Benefits in a Clonal Ant.” <i>Behavioral Ecology and Sociobiology</i>, vol. 68, no. 10, Springer, 2014, pp. 1701–10, doi:<a href=\"https://doi.org/10.1007/s00265-014-1778-8\">10.1007/s00265-014-1778-8</a>.","apa":"Westhus, C., Ugelvig, L. V., Tourdot, E., Heinze, J., Doums, C., &#38; Cremer, S. (2014). Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. <i>Behavioral Ecology and Sociobiology</i>. Springer. <a href=\"https://doi.org/10.1007/s00265-014-1778-8\">https://doi.org/10.1007/s00265-014-1778-8</a>"},"publication":"Behavioral Ecology and Sociobiology","related_material":{"record":[{"id":"9742","status":"public","relation":"research_data"}]},"title":"Increased grooming after repeated brood care provides sanitary benefits in a clonal ant","status":"public","date_updated":"2023-02-23T14:06:46Z","oa_version":"None","page":"1701 - 1710","publication_status":"published","day":"23","ec_funded":1,"abstract":[{"lang":"eng","text":"Repeated pathogen exposure is a common threat in colonies of social insects, posing selection pressures on colony members to respond with improved disease-defense performance. We here tested whether experience gained by repeated tending of low-level fungus-exposed (Metarhizium robertsii) larvae may alter the performance of sanitary brood care in the clonal ant, Platythyrea punctata. We trained ants individually over nine consecutive trials to either sham-treated or fungus-exposed larvae. We then compared the larval grooming behavior of naive and trained ants and measured how effectively they removed infectious fungal conidiospores from the fungus-exposed larvae. We found that the ants changed the duration of larval grooming in response to both, larval treatment and their level of experience: (1) sham-treated larvae received longer grooming than the fungus-exposed larvae and (2) trained ants performed less self-grooming but longer larval grooming than naive ants, which was true for both, ants trained to fungus-exposed and also to sham-treated larvae. Ants that groomed the fungus-exposed larvae for longer periods removed a higher number of fungal conidiospores from the surface of the fungus-exposed larvae. As experienced ants performed longer larval grooming, they were more effective in fungal removal, thus making them better caretakers under pathogen attack of the colony. By studying this clonal ant, we can thus conclude that even in the absence of genetic variation between colony members, differences in experience levels of brood care may affect performance of sanitary brood care in social insects."}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","article_processing_charge":"No","intvolume":"        68","date_created":"2018-12-11T11:56:03Z","acknowledgement":"We thank Katrin Kellner for colony establishment and characterization, Mike Bidochka for the fungal strain, Meghan Vyleta for fungal strain characterization, Martina Klatt and Simon Tragust for help in the laboratory, Dimitri Missoh for developing the software BioLogic, and Mark Brown and Raphaël Jeanson for discussion and help with data analysis. The study was funded by the European Research Council (ERC Starting Grant to SC; Marie Curie IEF to LVU) and the German Research Foundation DFG (to SC and to JH), and CW received funding by the doctoral school Diversité du Vivant (Cotutelle project to CD and SC).\r\n","department":[{"_id":"SyCr"}],"article_type":"original","volume":68,"month":"07","quality_controlled":"1","publication_identifier":{"issn":["0340-5443"]},"publist_id":"4823","type":"journal_article","language":[{"iso":"eng"}],"doi":"10.1007/s00265-014-1778-8","publisher":"Springer","year":"2014","date_published":"2014-07-23T00:00:00Z","author":[{"first_name":"Claudia","full_name":"Westhus, Claudia","last_name":"Westhus","id":"ca9c6ca9-e8aa-11ec-a586-b9471ede0494"},{"first_name":"Line V","full_name":"Ugelvig, Line V","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87","last_name":"Ugelvig","orcid":"0000-0003-1832-8883"},{"last_name":"Tourdot","full_name":"Tourdot, Edouard","first_name":"Edouard"},{"last_name":"Heinze","first_name":"Jürgen","full_name":"Heinze, Jürgen"},{"full_name":"Doums, Claudie","first_name":"Claudie","last_name":"Doums"},{"id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","orcid":"0000-0002-2193-3868","full_name":"Cremer, Sylvia","first_name":"Sylvia"}],"_id":"2161"},{"date_updated":"2021-01-12T06:56:11Z","status":"public","abstract":[{"text":"Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline, one cause of which may be pathogen spillover from managed pollinators like honeybees or commercial colonies of bumblebees. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.","lang":"eng"}],"publication_status":"published","oa_version":"Submitted Version","page":"364 - 366","day":"20","citation":{"ieee":"M. Fürst, D. Mcmahon, J. Osborne, R. Paxton, and M. Brown, “Disease associations between honeybees and bumblebees as a threat to wild pollinators,” <i>Nature</i>, vol. 506, no. 7488. Nature Publishing Group, pp. 364–366, 2014.","chicago":"Fürst, Matthias, Dino Mcmahon, Juliet Osborne, Robert Paxton, and Mark Brown. “Disease Associations between Honeybees and Bumblebees as a Threat to Wild Pollinators.” <i>Nature</i>. Nature Publishing Group, 2014. <a href=\"https://doi.org/10.1038/nature12977\">https://doi.org/10.1038/nature12977</a>.","ama":"Fürst M, Mcmahon D, Osborne J, Paxton R, Brown M. Disease associations between honeybees and bumblebees as a threat to wild pollinators. <i>Nature</i>. 2014;506(7488):364-366. doi:<a href=\"https://doi.org/10.1038/nature12977\">10.1038/nature12977</a>","apa":"Fürst, M., Mcmahon, D., Osborne, J., Paxton, R., &#38; Brown, M. (2014). Disease associations between honeybees and bumblebees as a threat to wild pollinators. <i>Nature</i>. Nature Publishing Group. <a href=\"https://doi.org/10.1038/nature12977\">https://doi.org/10.1038/nature12977</a>","ista":"Fürst M, Mcmahon D, Osborne J, Paxton R, Brown M. 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature. 506(7488), 364–366.","mla":"Fürst, Matthias, et al. “Disease Associations between Honeybees and Bumblebees as a Threat to Wild Pollinators.” <i>Nature</i>, vol. 506, no. 7488, Nature Publishing Group, 2014, pp. 364–66, doi:<a href=\"https://doi.org/10.1038/nature12977\">10.1038/nature12977</a>.","short":"M. Fürst, D. Mcmahon, J. Osborne, R. Paxton, M. Brown, Nature 506 (2014) 364–366."},"issue":"7488","scopus_import":1,"main_file_link":[{"url":"http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3985068/","open_access":"1"}],"title":"Disease associations between honeybees and bumblebees as a threat to wild pollinators","publication":"Nature","publisher":"Nature Publishing Group","year":"2014","language":[{"iso":"eng"}],"doi":"10.1038/nature12977","type":"journal_article","oa":1,"_id":"2235","author":[{"orcid":"0000-0002-3712-925X","id":"393B1196-F248-11E8-B48F-1D18A9856A87","last_name":"Fürst","full_name":"Fürst, Matthias","first_name":"Matthias"},{"last_name":"Mcmahon","full_name":"Mcmahon, Dino","first_name":"Dino"},{"last_name":"Osborne","first_name":"Juliet","full_name":"Osborne, Juliet"},{"last_name":"Paxton","full_name":"Paxton, Robert","first_name":"Robert"},{"full_name":"Brown, Mark","first_name":"Mark","last_name":"Brown"}],"date_published":"2014-02-20T00:00:00Z","department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:56:29Z","intvolume":"       506","user_id":"4435EBFC-F248-11E8-B48F-1D18A9856A87","quality_controlled":"1","publication_identifier":{"issn":["00280836"]},"publist_id":"4726","month":"02","volume":506},{"type":"dissertation","status":"public","year":"2014","publisher":"Institute of Science and Technology Austria","date_updated":"2023-09-07T11:38:56Z","language":[{"iso":"eng"}],"abstract":[{"text":"In this thesis I studied various individual and social immune defences employed by the invasive garden ant Lasius neglectus mostly against entomopathogenic fungi.  The first two chapters of this thesis address the phenomenon of 'social immunisation'. Social immunisation, that is the immunological protection of group members due to social contact to a pathogen-exposed nestmate, has been described in various social insect species against different types of pathogens. However, in the case of entomopathogenic fungi it has, so far, only been demonstrated that social immunisation exists at all. Its underlying mechanisms r any other properties were, however, unknown. In the first chapter of this thesis I identified the mechanistic basis of social immunisation in L. neglectus against the entomopathogenous fungus Metarhizium. I could show that nestmates of a pathogen-exposed individual contract low-level infections due to social interactions. These low-level infections are, however, non-lethal and cause an active stimulation of the immune system, which protects the nestmates upon subsequent pathogen encounters. In the second chapter of this thesis I investigated the specificity and colony level effects of social immunisation. I demonstrated that the protection conferred by social immunisation is highly specific, protecting ants only against the same pathogen strain. In addition, depending on the respective context, social immunisation may even cause fitness costs. I further showed that social immunisation crucially affects sanitary behaviour and disease dynamics within ant groups. In the third chapter of this thesis I studied the effects of the ectosymbiotic fungus Laboulbenia formicarum on its host L. neglectus. Although Laboulbeniales are the largest order of insect-parasitic fungi, research concerning host fitness consequence is sparse. I showed that highly Laboulbenia-infected ants sustain fitness costs under resource limitation, however, gain fitness benefits when exposed to an entomopathogenus fungus. These effects are probably cause by a prophylactic upregulation of behavioural as well as physiological immune defences in highly infected ants.","lang":"eng"}],"day":"01","page":"131","oa_version":"None","publication_status":"published","date_published":"2014-02-01T00:00:00Z","_id":"1395","degree_awarded":"PhD","author":[{"first_name":"Matthias","full_name":"Konrad, Matthias","last_name":"Konrad","id":"46528076-F248-11E8-B48F-1D18A9856A87"}],"alternative_title":["ISTA Thesis"],"article_processing_charge":"No","user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","citation":{"ieee":"M. Konrad, “Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus,” Institute of Science and Technology Austria, 2014.","chicago":"Konrad, Matthias. “Immune Defences in Ants: Effects of Social Immunisation and a Fungal Ectosymbiont in the Ant Lasius Neglectus.” Institute of Science and Technology Austria, 2014.","ama":"Konrad M. Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus. 2014.","ista":"Konrad M. 2014. Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus. Institute of Science and Technology Austria.","apa":"Konrad, M. (2014). <i>Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus</i>. Institute of Science and Technology Austria.","mla":"Konrad, Matthias. <i>Immune Defences in Ants: Effects of Social Immunisation and a Fungal Ectosymbiont in the Ant Lasius Neglectus</i>. Institute of Science and Technology Austria, 2014.","short":"M. Konrad, Immune Defences in Ants: Effects of Social Immunisation and a Fungal Ectosymbiont in the Ant Lasius Neglectus, Institute of Science and Technology Austria, 2014."},"department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:51:46Z","title":"Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus","supervisor":[{"orcid":"0000-0002-2193-3868","last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","full_name":"Cremer, Sylvia M","first_name":"Sylvia M"}],"publication_identifier":{"issn":["2663-337X"]},"publist_id":"5814","month":"02"},{"acknowledgement":"This work was funded by the DFG and the ERC.","citation":{"ieee":"M. Stock, “Evolution of a fungal pathogen towards individual versus social immunity in ants,” IST Austria, 2014.","chicago":"Stock, Miriam. “Evolution of a Fungal Pathogen towards Individual versus Social Immunity in Ants.” IST Austria, 2014.","ama":"Stock M. Evolution of a fungal pathogen towards individual versus social immunity in ants. 2014.","mla":"Stock, Miriam. <i>Evolution of a Fungal Pathogen towards Individual versus Social Immunity in Ants</i>. IST Austria, 2014.","short":"M. Stock, Evolution of a Fungal Pathogen towards Individual versus Social Immunity in Ants, IST Austria, 2014.","apa":"Stock, M. (2014). <i>Evolution of a fungal pathogen towards individual versus social immunity in ants</i>. IST Austria.","ista":"Stock M. 2014. Evolution of a fungal pathogen towards individual versus social immunity in ants. IST Austria."},"department":[{"_id":"SyCr"}],"date_created":"2018-12-11T11:51:49Z","alternative_title":["IST Austria Thesis"],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publist_id":"5803","month":"04","title":"Evolution of a fungal pathogen towards individual versus social immunity in ants","supervisor":[{"orcid":"0000-0002-2193-3868","last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","first_name":"Sylvia M","full_name":"Cremer, Sylvia M"}],"date_updated":"2021-01-12T06:50:30Z","publisher":"IST Austria","year":"2014","language":[{"iso":"eng"}],"type":"dissertation","status":"public","_id":"1404","author":[{"id":"42462816-F248-11E8-B48F-1D18A9856A87","last_name":"Stock","first_name":"Miriam","full_name":"Stock, Miriam"}],"abstract":[{"text":"The co-evolution of hosts and pathogens is characterized by continuous adaptations of both parties. Pathogens of social insects need to adapt towards disease defences at two levels: 1) individual immunity of each colony member consisting of behavioural defence strategies as well as humoral and cellular immune responses and 2) social immunity that is collectively performed by all group members comprising behavioural, physiological and organisational defence strategies.\r\n\r\nTo disentangle the selection pressure on pathogens by the collective versus individual level of disease defence in social insects, we performed an evolution experiment using the Argentine Ant, Linepithema humile, as a host and a mixture of the general insect pathogenic fungus Metarhizium spp. (6 strains) as a pathogen. We allowed pathogen evolution over 10 serial host passages to two different evolution host treatments: (1) only individual host immunity in a single host treatment, and (2) simultaneously acting individual and social immunity in a social host treatment, in which an exposed ant was accompanied by two untreated nestmates.\r\n\r\nBefore starting the pathogen evolution experiment, the 6 Metarhizium spp. strains were characterised concerning conidiospore size killing rates in singly and socially reared ants, their competitiveness under coinfecting conditions and their influence on ant behaviour. We analysed how the ancestral atrain mixture changed in conidiospere size, killing rate and strain composition dependent on host treatment (single or social hosts) during 10 passages and found that killing rate and conidiospere size of the pathogen increased under both evolution regimes, but different depending on host treatment.\r\n\r\nTesting the evolved strain mixtures that evolved under either the single or social host treatment under both single and social current rearing conditions in a full factorial design experiment revealed that the additional collective defences in insect societies add new selection pressure for their coevolving pathogens that compromise their ability to adapt to its host at the group level. To our knowledge, this is the first study directly measuring the influence of social immunity on pathogen evolution.","lang":"eng"}],"oa_version":"None","publication_status":"published","page":"101","date_published":"2014-04-01T00:00:00Z","day":"01"},{"status":"public","type":"research_data_reference","doi":"10.5061/dryad.vm0vc","year":"2014","publisher":"Dryad","date_updated":"2023-02-23T10:23:32Z","day":"13","oa_version":"Published Version","date_published":"2014-11-13T00:00:00Z","abstract":[{"text":"The fitness effects of symbionts on their hosts can be context-dependent, with usually benign symbionts causing detrimental effects when their hosts are stressed, or typically parasitic symbionts providing protection towards their hosts (e.g. against pathogen infection). Here, we studied the novel association between the invasive garden ant Lasius neglectus and its fungal ectosymbiont Laboulbenia formicarum for potential costs and benefits. We tested ants with different Laboulbenia levels for their survival and immunity under resource limitation and exposure to the obligate killing entomopathogen Metarhizium brunneum. While survival of L. neglectus workers under starvation was significantly decreased with increasing Laboulbenia levels, host survival under Metarhizium exposure increased with higher levels of the ectosymbiont, suggesting a symbiont-mediated anti-pathogen protection, which seems to be driven mechanistically by both improved sanitary behaviours and an upregulated immune system. Ants with high Laboulbenia levels showed significantly longer self-grooming and elevated expression of immune genes relevant for wound repair and antifungal responses (β-1,3-glucan binding protein, Prophenoloxidase), compared with ants carrying low Laboulbenia levels. This suggests that the ectosymbiont Laboulbenia formicarum weakens its ant host by either direct resource exploitation or the costs of an upregulated behavioural and immunological response, which, however, provides a prophylactic protection upon later exposure to pathogens.","lang":"eng"}],"author":[{"last_name":"Konrad","id":"46528076-F248-11E8-B48F-1D18A9856A87","full_name":"Konrad, Matthias","first_name":"Matthias"},{"first_name":"Anna V","full_name":"Grasse, Anna V","id":"406F989C-F248-11E8-B48F-1D18A9856A87","last_name":"Grasse"},{"id":"35A7A418-F248-11E8-B48F-1D18A9856A87","last_name":"Tragust","first_name":"Simon","full_name":"Tragust, Simon"},{"last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2193-3868","full_name":"Cremer, Sylvia","first_name":"Sylvia"}],"_id":"9740","oa":1,"article_processing_charge":"No","user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","date_created":"2021-07-28T08:38:40Z","department":[{"_id":"SyCr"}],"citation":{"chicago":"Konrad, Matthias, Anna V Grasse, Simon Tragust, and Sylvia Cremer. “Data from: Anti-Pathogen Protection versus Survival Costs Mediated by an Ectosymbiont in an Ant Host.” Dryad, 2014. <a href=\"https://doi.org/10.5061/dryad.vm0vc\">https://doi.org/10.5061/dryad.vm0vc</a>.","ieee":"M. Konrad, A. V. Grasse, S. Tragust, and S. Cremer, “Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host.” Dryad, 2014.","ista":"Konrad M, Grasse AV, Tragust S, Cremer S. 2014. Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host, Dryad, <a href=\"https://doi.org/10.5061/dryad.vm0vc\">10.5061/dryad.vm0vc</a>.","short":"M. Konrad, A.V. Grasse, S. Tragust, S. Cremer, (2014).","mla":"Konrad, Matthias, et al. <i>Data from: Anti-Pathogen Protection versus Survival Costs Mediated by an Ectosymbiont in an Ant Host</i>. Dryad, 2014, doi:<a href=\"https://doi.org/10.5061/dryad.vm0vc\">10.5061/dryad.vm0vc</a>.","apa":"Konrad, M., Grasse, A. V., Tragust, S., &#38; Cremer, S. (2014). Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Dryad. <a href=\"https://doi.org/10.5061/dryad.vm0vc\">https://doi.org/10.5061/dryad.vm0vc</a>","ama":"Konrad M, Grasse AV, Tragust S, Cremer S. Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. 2014. doi:<a href=\"https://doi.org/10.5061/dryad.vm0vc\">10.5061/dryad.vm0vc</a>"},"title":"Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host","related_material":{"record":[{"relation":"used_in_publication","status":"public","id":"1993"}]},"month":"11","main_file_link":[{"open_access":"1","url":"https://doi.org/10.5061/dryad.vm0vc"}]},{"day":"08","date_published":"2014-10-08T00:00:00Z","oa_version":"Published Version","abstract":[{"lang":"eng","text":"Background: The brood of ants and other social insects is highly susceptible to pathogens, particularly those that penetrate the soft larval and pupal cuticle. We here test whether the presence of a pupal cocoon, which occurs in some ant species but not in others, affects the sanitary brood care and fungal infection patterns after exposure to the entomopathogenic fungus Metarhizium brunneum. We use a) a comparative approach analysing four species with either naked or cocooned pupae and b) a within-species analysis of a single ant species, in which both pupal types co-exist in the same colony. Results: We found that the presence of a cocoon did not compromise fungal pathogen detection by the ants and that species with cocooned pupae increased brood grooming after pathogen exposure. All tested ant species further removed brood from their nests, which was predominantly expressed towards larvae and naked pupae treated with the live fungal pathogen. In contrast, cocooned pupae exposed to live fungus were not removed at higher rates than cocooned pupae exposed to dead fungus or a sham control. Consistent with this, exposure to the live fungus caused high numbers of infections and fungal outgrowth in larvae and naked pupae, but not in cocooned pupae. Moreover, the ants consistently removed the brood prior to fungal outgrowth, ensuring a clean brood chamber. Conclusion: Our study suggests that the pupal cocoon has a protective effect against fungal infection, causing an adaptive change in sanitary behaviours by the ants. It further demonstrates that brood removal - originally described for honeybees as “hygienic behaviour” – is a widespread sanitary behaviour in ants, which likely has important implications on disease dynamics in social insect colonies."}],"author":[{"full_name":"Tragust, Simon","first_name":"Simon","last_name":"Tragust","id":"35A7A418-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Ugelvig, Line V","first_name":"Line V","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87","last_name":"Ugelvig","orcid":"0000-0003-1832-8883"},{"first_name":"Michel","full_name":"Chapuisat, Michel","last_name":"Chapuisat"},{"full_name":"Heinze, Jürgen","first_name":"Jürgen","last_name":"Heinze"},{"last_name":"Cremer","id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2193-3868","first_name":"Sylvia","full_name":"Cremer, Sylvia"}],"_id":"9753","oa":1,"status":"public","type":"research_data_reference","doi":"10.5061/dryad.nc0gc","year":"2014","date_updated":"2023-02-23T10:36:17Z","publisher":"Dryad","title":"Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies","related_material":{"record":[{"relation":"used_in_publication","status":"public","id":"2284"}]},"month":"10","main_file_link":[{"url":"https://doi.org/10.5061/dryad.nc0gc","open_access":"1"}],"user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","article_processing_charge":"No","date_created":"2021-07-30T08:24:11Z","citation":{"ista":"Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S. 2014. Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies, Dryad, <a href=\"https://doi.org/10.5061/dryad.nc0gc\">10.5061/dryad.nc0gc</a>.","apa":"Tragust, S., Ugelvig, L. V., Chapuisat, M., Heinze, J., &#38; Cremer, S. (2014). Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies. Dryad. <a href=\"https://doi.org/10.5061/dryad.nc0gc\">https://doi.org/10.5061/dryad.nc0gc</a>","mla":"Tragust, Simon, et al. <i>Data from: Pupal Cocoons Affect Sanitary Brood Care and Limit Fungal Infections in Ant Colonies</i>. Dryad, 2014, doi:<a href=\"https://doi.org/10.5061/dryad.nc0gc\">10.5061/dryad.nc0gc</a>.","short":"S. Tragust, L.V. Ugelvig, M. Chapuisat, J. Heinze, S. Cremer, (2014).","ama":"Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S. Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies. 2014. doi:<a href=\"https://doi.org/10.5061/dryad.nc0gc\">10.5061/dryad.nc0gc</a>","chicago":"Tragust, Simon, Line V Ugelvig, Michel Chapuisat, Jürgen Heinze, and Sylvia Cremer. “Data from: Pupal Cocoons Affect Sanitary Brood Care and Limit Fungal Infections in Ant Colonies.” Dryad, 2014. <a href=\"https://doi.org/10.5061/dryad.nc0gc\">https://doi.org/10.5061/dryad.nc0gc</a>.","ieee":"S. Tragust, L. V. Ugelvig, M. Chapuisat, J. Heinze, and S. Cremer, “Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies.” Dryad, 2014."},"department":[{"_id":"SyCr"}]},{"month":"08","title":"Supporting information","related_material":{"record":[{"status":"public","id":"2086","relation":"used_in_publication"}]},"department":[{"_id":"SyCr"}],"citation":{"ieee":"S. Wolf <i>et al.</i>, “Supporting information.” Public Library of Science, 2014.","chicago":"Wolf, Stephan, Dino Mcmahon, Ka Lim, Christopher Pull, Suzanne Clark, Robert Paxton, and Juliet Osborne. “Supporting Information.” Public Library of Science, 2014. <a href=\"https://doi.org/10.1371/journal.pone.0103989.s003\">https://doi.org/10.1371/journal.pone.0103989.s003</a>.","ama":"Wolf S, Mcmahon D, Lim K, et al. Supporting information. 2014. doi:<a href=\"https://doi.org/10.1371/journal.pone.0103989.s003\">10.1371/journal.pone.0103989.s003</a>","ista":"Wolf S, Mcmahon D, Lim K, Pull C, Clark S, Paxton R, Osborne J. 2014. Supporting information, Public Library of Science, <a href=\"https://doi.org/10.1371/journal.pone.0103989.s003\">10.1371/journal.pone.0103989.s003</a>.","short":"S. Wolf, D. Mcmahon, K. Lim, C. Pull, S. Clark, R. Paxton, J. Osborne, (2014).","mla":"Wolf, Stephan, et al. <i>Supporting Information</i>. Public Library of Science, 2014, doi:<a href=\"https://doi.org/10.1371/journal.pone.0103989.s003\">10.1371/journal.pone.0103989.s003</a>.","apa":"Wolf, S., Mcmahon, D., Lim, K., Pull, C., Clark, S., Paxton, R., &#38; Osborne, J. (2014). Supporting information. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pone.0103989.s003\">https://doi.org/10.1371/journal.pone.0103989.s003</a>"},"date_created":"2021-08-11T14:17:53Z","article_processing_charge":"No","user_id":"6785fbc1-c503-11eb-8a32-93094b40e1cf","_id":"9888","author":[{"first_name":"Stephan","full_name":"Wolf, Stephan","last_name":"Wolf"},{"first_name":"Dino","full_name":"Mcmahon, Dino","last_name":"Mcmahon"},{"last_name":"Lim","full_name":"Lim, Ka","first_name":"Ka"},{"full_name":"Pull, Christopher","first_name":"Christopher","orcid":"0000-0003-1122-3982","id":"3C7F4840-F248-11E8-B48F-1D18A9856A87","last_name":"Pull"},{"last_name":"Clark","first_name":"Suzanne","full_name":"Clark, Suzanne"},{"last_name":"Paxton","first_name":"Robert","full_name":"Paxton, Robert"},{"last_name":"Osborne","full_name":"Osborne, Juliet","first_name":"Juliet"}],"abstract":[{"lang":"eng","text":"Detailed description of the experimental prodedures, data analyses and additional statistical analyses of the results."}],"day":"06","oa_version":"Published Version","year":"2014","publisher":"Public Library of Science","date_updated":"2023-02-23T10:27:38Z","doi":"10.1371/journal.pone.0103989.s003","type":"research_data_reference","status":"public"},{"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","intvolume":"        23","date_created":"2018-12-11T12:00:23Z","acknowledgement":"Funding for this project was obtained by the German Research Foundation (DFG, to S.C.) and the European Research Council (ERC, through an ERC-Starting Grant to S.C. and an Individual Marie Curie IEF fellowship to L.V.U.).\r\nWe thank Jørgen Eilenberg, Bernhardt Steinwender, Miriam Stock, and Meghan L. Vyleta for the fungal strain and its characterization; Volker Witte for chemical information; Eva Sixt for ant drawings; and Robert Hauschild for help with image analysis. We further thank Martin Kaltenpoth, Michael Sixt, Jürgen Heinze, and Joachim Ruther for discussion and Daria Siekhaus, Sophie A.O. Armitage, and Leila Masri for comments on the manuscript. \r\n","department":[{"_id":"SyCr"},{"_id":"CaHe"}],"volume":23,"month":"01","quality_controlled":"1","publist_id":"3811","type":"journal_article","language":[{"iso":"eng"}],"doi":"10.1016/j.cub.2012.11.034","publisher":"Cell Press","year":"2013","date_published":"2013-01-07T00:00:00Z","author":[{"first_name":"Simon","full_name":"Tragust, Simon","id":"35A7A418-F248-11E8-B48F-1D18A9856A87","last_name":"Tragust"},{"id":"479DDAAC-E9CD-11E9-9B5F-82450873F7A1","last_name":"Mitteregger","full_name":"Mitteregger, Barbara","first_name":"Barbara"},{"first_name":"Vanessa","full_name":"Barone, Vanessa","orcid":"0000-0003-2676-3367","last_name":"Barone","id":"419EECCC-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Matthias","full_name":"Konrad, Matthias","last_name":"Konrad","id":"46528076-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Line V","full_name":"Ugelvig, Line V","last_name":"Ugelvig","id":"3DC97C8E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1832-8883"},{"id":"2F64EC8C-F248-11E8-B48F-1D18A9856A87","last_name":"Cremer","orcid":"0000-0002-2193-3868","first_name":"Sylvia","full_name":"Cremer, Sylvia"}],"_id":"2926","issue":"1","scopus_import":1,"project":[{"grant_number":"CR-118/3-1","_id":"25DAF0B2-B435-11E9-9278-68D0E5697425","name":"Host-Parasite Coevolution"},{"name":"Social Vaccination in Ant Colonies: from Individual Mechanisms to Society Effects","_id":"25DC711C-B435-11E9-9278-68D0E5697425","grant_number":"243071","call_identifier":"FP7"},{"grant_number":"302004","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"}],"citation":{"ieee":"S. Tragust, B. Mitteregger, V. Barone, M. Konrad, L. V. Ugelvig, and S. Cremer, “Ants disinfect fungus-exposed brood by oral uptake and spread of their poison,” <i>Current Biology</i>, vol. 23, no. 1. Cell Press, pp. 76–82, 2013.","chicago":"Tragust, Simon, Barbara Mitteregger, Vanessa Barone, Matthias Konrad, Line V Ugelvig, and Sylvia Cremer. “Ants Disinfect Fungus-Exposed Brood by Oral Uptake and Spread of Their Poison.” <i>Current Biology</i>. Cell Press, 2013. <a href=\"https://doi.org/10.1016/j.cub.2012.11.034\">https://doi.org/10.1016/j.cub.2012.11.034</a>.","ama":"Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. <i>Current Biology</i>. 2013;23(1):76-82. doi:<a href=\"https://doi.org/10.1016/j.cub.2012.11.034\">10.1016/j.cub.2012.11.034</a>","ista":"Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. 2013. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Current Biology. 23(1), 76–82.","apa":"Tragust, S., Mitteregger, B., Barone, V., Konrad, M., Ugelvig, L. V., &#38; Cremer, S. (2013). Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. <i>Current Biology</i>. Cell Press. <a href=\"https://doi.org/10.1016/j.cub.2012.11.034\">https://doi.org/10.1016/j.cub.2012.11.034</a>","mla":"Tragust, Simon, et al. “Ants Disinfect Fungus-Exposed Brood by Oral Uptake and Spread of Their Poison.” <i>Current Biology</i>, vol. 23, no. 1, Cell Press, 2013, pp. 76–82, doi:<a href=\"https://doi.org/10.1016/j.cub.2012.11.034\">10.1016/j.cub.2012.11.034</a>.","short":"S. Tragust, B. Mitteregger, V. Barone, M. Konrad, L.V. Ugelvig, S. Cremer, Current Biology 23 (2013) 76–82."},"publication":"Current Biology","related_material":{"record":[{"relation":"research_data","id":"9757","status":"public"},{"relation":"dissertation_contains","status":"public","id":"961"}]},"title":"Ants disinfect fungus-exposed brood by oral uptake and spread of their poison","status":"public","date_updated":"2023-09-07T12:05:08Z","page":"76 - 82","publication_status":"published","oa_version":"None","day":"07","ec_funded":1,"abstract":[{"lang":"eng","text":"To fight infectious diseases, host immune defenses are employed at multiple levels. Sanitary behavior, such as pathogen avoidance and removal, acts as a first line of defense to prevent infection [1] before activation of the physiological immune system. Insect societies have evolved a wide range of collective hygiene measures and intensive health care toward pathogen-exposed group members [2]. One of the most common behaviors is allogrooming, in which nestmates remove infectious particles from the body surfaces of exposed individuals [3]. Here we show that, in invasive garden ants, grooming of fungus-exposed brood is effective beyond the sheer mechanical removal of fungal conidiospores; it also includes chemical disinfection through the application of poison produced by the ants themselves. Formic acid is the main active component of the poison. It inhibits fungal growth of conidiospores remaining on the brood surface after grooming and also those collected in the mouth of the grooming ant. This dual function is achieved by uptake of the poison droplet into the mouth through acidopore self-grooming and subsequent application onto the infectious brood via brood grooming. This extraordinary behavior extends the current understanding of grooming and the establishment of social immunity in insect societies."}]},{"abstract":[{"text":"Pathogens exert a strong selection pressure on organisms to evolve effective immune defences. In addition to individual immunity, social organisms can act cooperatively to produce collective defences. In many ant species, queens have the option to found a colony alone or in groups with other, often unrelated, conspecifics. These associations are transient, usually lasting only as long as each queen benefits from the presence of others. In fact, once the first workers emerge, queens fight to the death for dominance. One potential advantage of co-founding may be that queens benefit from collective disease defences, such as mutual grooming, that act against common soil pathogens. We test this hypothesis by exposing single and co-founding queens to a fungal parasite, in order to assess whether queens in co-founding associations have improved survival. Surprisingly, co-foundresses exposed to the entomopathogenic fungus Metarhizium did not engage in cooperative disease defences, and consequently, we find no direct benefit of multiple queens on survival. However, an indirect benefit was observed, with parasite-exposed queens producing more brood when they co-founded, than when they were alone. We suggest this is due to a trade-off between reproduction and immunity. Additionally, we report an extraordinary ability of the queens to tolerate an infection for long periods after parasite exposure. Our study suggests that there are no social immunity benefits for co-founding ant queens, but that in parasite-rich environments, the presence of additional queens may nevertheless improve the chances of colony founding success.","lang":"eng"}],"page":"1125  - 1136","oa_version":"None","publication_status":"published","date_published":"2013-11-14T00:00:00Z","day":"14","_id":"2283","author":[{"last_name":"Pull","id":"3C7F4840-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1122-3982","first_name":"Christopher","full_name":"Pull, Christopher"},{"full_name":"Hughes, William","first_name":"William","last_name":"Hughes"},{"last_name":"Brown","id":"3DAB9AFC-F248-11E8-B48F-1D18A9856A87","first_name":"Markus","full_name":"Brown, Markus"}],"type":"journal_article","status":"public","date_updated":"2021-01-12T06:56:31Z","publisher":"Springer","year":"2013","language":[{"iso":"eng"}],"doi":"10.1007/s00114-013-1115-5","volume":100,"title":"Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger ","publication":"Naturwissenschaften","quality_controlled":"1","publist_id":"4649","month":"11","intvolume":"       100","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","issue":"12","scopus_import":1,"department":[{"_id":"SyCr"}],"citation":{"ieee":"C. Pull, W. Hughes, and M. Brown, “Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger ,” <i>Naturwissenschaften</i>, vol. 100, no. 12. Springer, pp. 1125–1136, 2013.","chicago":"Pull, Christopher, William Hughes, and Markus Brown. “Tolerating an Infection: An Indirect Benefit of Co-Founding Queen Associations in the Ant Lasius Niger .” <i>Naturwissenschaften</i>. Springer, 2013. <a href=\"https://doi.org/10.1007/s00114-013-1115-5\">https://doi.org/10.1007/s00114-013-1115-5</a>.","ama":"Pull C, Hughes W, Brown M. Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger . <i>Naturwissenschaften</i>. 2013;100(12):1125-1136. doi:<a href=\"https://doi.org/10.1007/s00114-013-1115-5\">10.1007/s00114-013-1115-5</a>","apa":"Pull, C., Hughes, W., &#38; Brown, M. (2013). Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger . <i>Naturwissenschaften</i>. Springer. <a href=\"https://doi.org/10.1007/s00114-013-1115-5\">https://doi.org/10.1007/s00114-013-1115-5</a>","ista":"Pull C, Hughes W, Brown M. 2013. Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger . Naturwissenschaften. 100(12), 1125–1136.","mla":"Pull, Christopher, et al. “Tolerating an Infection: An Indirect Benefit of Co-Founding Queen Associations in the Ant Lasius Niger .” <i>Naturwissenschaften</i>, vol. 100, no. 12, Springer, 2013, pp. 1125–36, doi:<a href=\"https://doi.org/10.1007/s00114-013-1115-5\">10.1007/s00114-013-1115-5</a>.","short":"C. Pull, W. Hughes, M. Brown, Naturwissenschaften 100 (2013) 1125–1136."},"date_created":"2018-12-11T11:56:45Z"}]
