---
_id: '12543'
abstract:
- lang: eng
text: Treating sick group members is a hallmark of collective disease defence in
vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness
and epidemiology, it is still largely unknown how pathogens react to the selection
pressure imposed by care intervention. Using social insects and pathogenic fungi,
we here performed a serial passage experiment in the presence or absence of colony
members, which provide social immunity by grooming off infectious spores from
exposed individuals. We found specific effects on pathogen diversity, virulence
and transmission. Under selection of social immunity, pathogens invested into
higher spore production, but spores were less virulent. Notably, they also elicited
a lower grooming response in colony members, compared with spores from the individual
host selection lines. Chemical spore analysis suggested that the spores from social
selection lines escaped the caregivers’ detection by containing lower levels of
ergosterol, a key fungal membrane component. Experimental application of chemically
pure ergosterol indeed induced sanitary grooming, supporting its role as a microbe-associated
cue triggering host social immunity against fungal pathogens. By reducing this
detection cue, pathogens were able to evade the otherwise very effective collective
disease defences of their social hosts.
acknowledged_ssus:
- _id: LifeSc
acknowledgement: We thank B. M. Steinwender, N. V. Meyling and J. Eilenberg for the
fungal strains; J. Anaya-Rojas for statistical advice; the Social Immunity team
at ISTA for ant collection and experimental help, in particular H. Leitner, and
the ISTA Lab Support Facility for general laboratory support; D. Ebert, H. Schulenburg
and J. Heinze for continued project discussion; and M. Sixt, R. Roemhild and the
Social Immunity team for comments on the manuscript. The study was funded by the
German Research Foundation (CR118/3-1) within the Framework of the Priority Program
SPP 1399, and the European Research Council (ERC) under the European Union’s Horizon
2020 Research and Innovation Programme (No. 771402; EPIDEMICSonCHIP), both to S.C.
article_processing_charge: No
article_type: original
author:
- first_name: Miriam
full_name: Stock, Miriam
id: 42462816-F248-11E8-B48F-1D18A9856A87
last_name: Stock
- first_name: Barbara
full_name: Milutinovic, Barbara
id: 2CDC32B8-F248-11E8-B48F-1D18A9856A87
last_name: Milutinovic
orcid: 0000-0002-8214-4758
- first_name: Michaela
full_name: Hönigsberger, Michaela
id: 953894f3-25bd-11ec-8556-f70a9d38ef60
last_name: Hönigsberger
- first_name: Anna V
full_name: Grasse, Anna V
id: 406F989C-F248-11E8-B48F-1D18A9856A87
last_name: Grasse
- first_name: Florian
full_name: Wiesenhofer, Florian
id: 39523C54-F248-11E8-B48F-1D18A9856A87
last_name: Wiesenhofer
- first_name: Niklas
full_name: Kampleitner, Niklas
id: 2AC57FAC-F248-11E8-B48F-1D18A9856A87
last_name: Kampleitner
- first_name: Madhumitha
full_name: Narasimhan, Madhumitha
id: 44BF24D0-F248-11E8-B48F-1D18A9856A87
last_name: Narasimhan
orcid: 0000-0002-8600-0671
- first_name: Thomas
full_name: Schmitt, Thomas
last_name: Schmitt
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Stock M, Milutinovic B, Hönigsberger M, et al. Pathogen evasion of social immunity.
Nature Ecology and Evolution. 2023;7:450-460. doi:10.1038/s41559-023-01981-6
apa: Stock, M., Milutinovic, B., Hönigsberger, M., Grasse, A. V., Wiesenhofer, F.,
Kampleitner, N., … Cremer, S. (2023). Pathogen evasion of social immunity. Nature
Ecology and Evolution. Springer Nature. https://doi.org/10.1038/s41559-023-01981-6
chicago: Stock, Miriam, Barbara Milutinovic, Michaela Hönigsberger, Anna V Grasse,
Florian Wiesenhofer, Niklas Kampleitner, Madhumitha Narasimhan, Thomas Schmitt,
and Sylvia Cremer. “Pathogen Evasion of Social Immunity.” Nature Ecology and
Evolution. Springer Nature, 2023. https://doi.org/10.1038/s41559-023-01981-6.
ieee: M. Stock et al., “Pathogen evasion of social immunity,” Nature Ecology
and Evolution, vol. 7. Springer Nature, pp. 450–460, 2023.
ista: Stock M, Milutinovic B, Hönigsberger M, Grasse AV, Wiesenhofer F, Kampleitner
N, Narasimhan M, Schmitt T, Cremer S. 2023. Pathogen evasion of social immunity.
Nature Ecology and Evolution. 7, 450–460.
mla: Stock, Miriam, et al. “Pathogen Evasion of Social Immunity.” Nature Ecology
and Evolution, vol. 7, Springer Nature, 2023, pp. 450–60, doi:10.1038/s41559-023-01981-6.
short: M. Stock, B. Milutinovic, M. Hönigsberger, A.V. Grasse, F. Wiesenhofer, N.
Kampleitner, M. Narasimhan, T. Schmitt, S. Cremer, Nature Ecology and Evolution
7 (2023) 450–460.
date_created: 2023-02-12T23:00:59Z
date_published: 2023-03-01T00:00:00Z
date_updated: 2023-08-16T11:55:48Z
day: '01'
ddc:
- '570'
department:
- _id: SyCr
- _id: LifeSc
- _id: JiFr
doi: 10.1038/s41559-023-01981-6
ec_funded: 1
external_id:
isi:
- '000924572800001'
pmid:
- '36732670'
file:
- access_level: open_access
checksum: 8244f4650a0e7aeea488d1bcd4a31702
content_type: application/pdf
creator: dernst
date_created: 2023-08-16T11:54:59Z
date_updated: 2023-08-16T11:54:59Z
file_id: '14069'
file_name: 2023_NatureEcoEvo_Stock.pdf
file_size: 1600499
relation: main_file
success: 1
file_date_updated: 2023-08-16T11:54:59Z
has_accepted_license: '1'
intvolume: ' 7'
isi: 1
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
page: 450-460
pmid: 1
project:
- _id: 2649B4DE-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '771402'
name: Epidemics in ant societies on a chip
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: Nature Ecology and Evolution
publication_identifier:
eissn:
- 2397-334X
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
related_material:
link:
- description: News on ISTA website
relation: press_release
url: https://ista.ac.at/en/news/how-sneaky-germs-hide-from-ants/
scopus_import: '1'
status: public
title: Pathogen evasion of social immunity
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 7
year: '2023'
...
---
_id: '7343'
abstract:
- lang: eng
text: Coinfections with multiple pathogens can result in complex within‐host dynamics
affecting virulence and transmission. While multiple infections are intensively
studied in solitary hosts, it is so far unresolved how social host interactions
interfere with pathogen competition, and if this depends on coinfection diversity.
We studied how the collective disease defences of ants – their social immunity
– influence pathogen competition in coinfections of same or different fungal pathogen
species. Social immunity reduced virulence for all pathogen combinations, but
interfered with spore production only in different‐species coinfections. Here,
it decreased overall pathogen sporulation success while increasing co‐sporulation
on individual cadavers and maintaining a higher pathogen diversity at the community
level. Mathematical modelling revealed that host sanitary care alone can modulate
competitive outcomes between pathogens, giving advantage to fast‐germinating,
thus less grooming‐sensitive ones. Host social interactions can hence modulate
infection dynamics in coinfected group members, thereby altering pathogen communities
at the host level and population level.
acknowledged_ssus:
- _id: LifeSc
acknowledgement: "We thank Bernhardt Steinwender and Jorgen Eilenberg for the fungal
strains, Xavier Espadaler, Mireia Diaz, Christiane Wanke, Lumi Viljakainen and the
Social Immunity Team at IST Austria, for help with ant collection, and Wanda Gorecka
and Gertraud Stift of the IST Austria Life Science Facility for technical support.
We are thankful to Dieter Ebert for input at all stages of the project, Roger Mundry
for statistical advice, Hinrich Schulenburg, Paul Schmid-Hempel, Yuko\r\nUlrich
and Joachim Kurtz for project discussion, Bor Kavcic for advice on growth curves,
Marcus Roper for advice on modelling work and comments on the manuscript, as well
as Marjon de Vos, Weini Huang and the Social Immunity Team for comments on the manuscript.\r\nThis
study was funded by the German Research Foundation (DFG) within the Priority Programme
1399 Host-parasite Coevolution (CR 118/3 to S.C.) and the People Programme\r\n(Marie
Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013)
under REA grant agreement no 291734 (ISTFELLOW to B.M.). "
article_processing_charge: Yes (via OA deal)
article_type: letter_note
author:
- first_name: Barbara
full_name: Milutinovic, Barbara
id: 2CDC32B8-F248-11E8-B48F-1D18A9856A87
last_name: Milutinovic
orcid: 0000-0002-8214-4758
- first_name: Miriam
full_name: Stock, Miriam
id: 42462816-F248-11E8-B48F-1D18A9856A87
last_name: Stock
- first_name: Anna V
full_name: Grasse, Anna V
id: 406F989C-F248-11E8-B48F-1D18A9856A87
last_name: Grasse
- first_name: Elisabeth
full_name: Naderlinger, Elisabeth
id: 31757262-F248-11E8-B48F-1D18A9856A87
last_name: Naderlinger
- first_name: Christian
full_name: Hilbe, Christian
id: 2FDF8F3C-F248-11E8-B48F-1D18A9856A87
last_name: Hilbe
orcid: 0000-0001-5116-955X
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Milutinovic B, Stock M, Grasse AV, Naderlinger E, Hilbe C, Cremer S. Social
immunity modulates competition between coinfecting pathogens. Ecology Letters.
2020;23(3):565-574. doi:10.1111/ele.13458
apa: Milutinovic, B., Stock, M., Grasse, A. V., Naderlinger, E., Hilbe, C., &
Cremer, S. (2020). Social immunity modulates competition between coinfecting pathogens.
Ecology Letters. Wiley. https://doi.org/10.1111/ele.13458
chicago: Milutinovic, Barbara, Miriam Stock, Anna V Grasse, Elisabeth Naderlinger,
Christian Hilbe, and Sylvia Cremer. “Social Immunity Modulates Competition between
Coinfecting Pathogens.” Ecology Letters. Wiley, 2020. https://doi.org/10.1111/ele.13458.
ieee: B. Milutinovic, M. Stock, A. V. Grasse, E. Naderlinger, C. Hilbe, and S. Cremer,
“Social immunity modulates competition between coinfecting pathogens,” Ecology
Letters, vol. 23, no. 3. Wiley, pp. 565–574, 2020.
ista: Milutinovic B, Stock M, Grasse AV, Naderlinger E, Hilbe C, Cremer S. 2020.
Social immunity modulates competition between coinfecting pathogens. Ecology Letters.
23(3), 565–574.
mla: Milutinovic, Barbara, et al. “Social Immunity Modulates Competition between
Coinfecting Pathogens.” Ecology Letters, vol. 23, no. 3, Wiley, 2020, pp.
565–74, doi:10.1111/ele.13458.
short: B. Milutinovic, M. Stock, A.V. Grasse, E. Naderlinger, C. Hilbe, S. Cremer,
Ecology Letters 23 (2020) 565–574.
date_created: 2020-01-20T13:32:12Z
date_published: 2020-03-01T00:00:00Z
date_updated: 2023-09-05T16:04:49Z
day: '01'
ddc:
- '570'
department:
- _id: SyCr
- _id: KrCh
doi: 10.1111/ele.13458
ec_funded: 1
external_id:
isi:
- '000507515900001'
file:
- access_level: open_access
checksum: 0cd8be386fa219db02845b7c3991ce04
content_type: application/pdf
creator: dernst
date_created: 2020-11-19T11:27:10Z
date_updated: 2020-11-19T11:27:10Z
file_id: '8776'
file_name: 2020_EcologyLetters_Milutinovic.pdf
file_size: 561749
relation: main_file
success: 1
file_date_updated: 2020-11-19T11:27:10Z
has_accepted_license: '1'
intvolume: ' 23'
isi: 1
issue: '3'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc/4.0/
month: '03'
oa: 1
oa_version: Published Version
page: 565-574
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '291734'
name: International IST Postdoc Fellowship Programme
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: Ecology Letters
publication_identifier:
eissn:
- 1461-0248
issn:
- 1461-023X
publication_status: published
publisher: Wiley
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
url: https://ist.ac.at/en/news/social-ants-shapes-disease-outcome/
record:
- id: '13060'
relation: research_data
status: public
scopus_import: '1'
status: public
title: Social immunity modulates competition between coinfecting pathogens
tmp:
image: /images/cc_by_nc.png
legal_code_url: https://creativecommons.org/licenses/by-nc/4.0/legalcode
name: Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
short: CC BY-NC (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 23
year: '2020'
...
---
_id: '1202'
acknowledgement: The authors thank Sophie A.O. Armitage and Jan N. Offenborn for helpful
comments on the figures, and two anonymous reviewers for their helpful comments.
The project was funded by the Deutsche Forschungsgemeinschaft (DFG, KU 1929/4-2)
within the priority programme SPP 1399 “Host–Parasite Coevolution”.
author:
- first_name: Barbara
full_name: Milutinovic, Barbara
id: 2CDC32B8-F248-11E8-B48F-1D18A9856A87
last_name: Milutinovic
orcid: 0000-0002-8214-4758
- first_name: Robert
full_name: Peuß, Robert
last_name: Peuß
- first_name: Kevin
full_name: Ferro, Kevin
last_name: Ferro
- first_name: Joachim
full_name: Kurtz, Joachim
last_name: Kurtz
citation:
ama: 'Milutinovic B, Peuß R, Ferro K, Kurtz J. Immune priming in arthropods: an
update focusing on the red flour beetle. Zoology . 2016;119(4):254-261.
doi:10.1016/j.zool.2016.03.006'
apa: 'Milutinovic, B., Peuß, R., Ferro, K., & Kurtz, J. (2016). Immune priming
in arthropods: an update focusing on the red flour beetle. Zoology . Elsevier.
https://doi.org/10.1016/j.zool.2016.03.006'
chicago: 'Milutinovic, Barbara, Robert Peuß, Kevin Ferro, and Joachim Kurtz. “Immune
Priming in Arthropods: An Update Focusing on the Red Flour Beetle.” Zoology
. Elsevier, 2016. https://doi.org/10.1016/j.zool.2016.03.006.'
ieee: 'B. Milutinovic, R. Peuß, K. Ferro, and J. Kurtz, “Immune priming in arthropods:
an update focusing on the red flour beetle,” Zoology , vol. 119, no. 4.
Elsevier, pp. 254–261, 2016.'
ista: 'Milutinovic B, Peuß R, Ferro K, Kurtz J. 2016. Immune priming in arthropods:
an update focusing on the red flour beetle. Zoology . 119(4), 254–261.'
mla: 'Milutinovic, Barbara, et al. “Immune Priming in Arthropods: An Update Focusing
on the Red Flour Beetle.” Zoology , vol. 119, no. 4, Elsevier, 2016, pp.
254–61, doi:10.1016/j.zool.2016.03.006.'
short: B. Milutinovic, R. Peuß, K. Ferro, J. Kurtz, Zoology 119 (2016) 254–261.
date_created: 2018-12-11T11:50:41Z
date_published: 2016-08-01T00:00:00Z
date_updated: 2021-01-12T06:49:03Z
day: '01'
ddc:
- '570'
department:
- _id: SyCr
doi: 10.1016/j.zool.2016.03.006
file:
- access_level: open_access
checksum: 8396d5bd95f9c4295857162f902afabf
content_type: application/pdf
creator: kschuh
date_created: 2019-01-25T13:00:20Z
date_updated: 2020-07-14T12:44:39Z
file_id: '5885'
file_name: 2016_Elsevier_Milutinovic.pdf
file_size: 1473211
relation: main_file
file_date_updated: 2020-07-14T12:44:39Z
has_accepted_license: '1'
intvolume: ' 119'
issue: '4'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '08'
oa: 1
oa_version: Published Version
page: 254 - 261
project:
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: 'Zoology '
publication_status: published
publisher: Elsevier
publist_id: '6147'
quality_controlled: '1'
scopus_import: 1
status: public
title: 'Immune priming in arthropods: an update focusing on the red flour beetle'
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 3E5EF7F0-F248-11E8-B48F-1D18A9856A87
volume: 119
year: '2016'
...
---
_id: '1993'
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
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."
article_number: '20141976'
article_processing_charge: No
article_type: original
author:
- first_name: Matthias
full_name: Konrad, Matthias
id: 46528076-F248-11E8-B48F-1D18A9856A87
last_name: Konrad
- 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
id: 35A7A418-F248-11E8-B48F-1D18A9856A87
last_name: Tragust
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Konrad M, Grasse AV, Tragust S, Cremer S. 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. 2015;282(1799). doi:10.1098/rspb.2014.1976
apa: Konrad, M., Grasse, A. V., 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. The Royal Society.
https://doi.org/10.1098/rspb.2014.1976
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.”
Proceedings of the Royal Society of London Series B Biological Sciences.
The Royal Society, 2015. https://doi.org/10.1098/rspb.2014.1976.
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,” Proceedings
of the Royal Society of London Series B Biological Sciences, vol. 282, no.
1799. The Royal Society, 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.
mla: Konrad, Matthias, et al. “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, vol. 282, no. 1799, 20141976, The Royal Society,
2015, doi:10.1098/rspb.2014.1976.
short: M. Konrad, A.V. Grasse, S. Tragust, S. Cremer, Proceedings of the Royal Society
of London Series B Biological Sciences 282 (2015).
date_created: 2018-12-11T11:55:06Z
date_published: 2015-01-22T00:00:00Z
date_updated: 2023-02-23T14:06:41Z
day: '22'
department:
- _id: SyCr
doi: 10.1098/rspb.2014.1976
ec_funded: 1
external_id:
pmid:
- '25473011'
intvolume: ' 282'
issue: '1799'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4286035/
month: '01'
oa: 1
oa_version: Submitted Version
pmid: 1
project:
- _id: 25DC711C-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '243071'
name: 'Social Vaccination in Ant Colonies: from Individual Mechanisms to Society
Effects'
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: Proceedings of the Royal Society of London Series B Biological Sciences
publication_identifier:
eissn:
- 1471-2954
issn:
- 0962-8452
publication_status: published
publisher: The Royal Society
publist_id: '5090'
quality_controlled: '1'
related_material:
record:
- id: '9740'
relation: research_data
status: public
scopus_import: '1'
status: public
title: Anti-pathogen protection versus survival costs mediated by an ectosymbiont
in an ant host
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 282
year: '2015'
...
---
_id: '2161'
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.'
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"
article_processing_charge: No
article_type: original
author:
- first_name: Claudia
full_name: Westhus, Claudia
id: ca9c6ca9-e8aa-11ec-a586-b9471ede0494
last_name: Westhus
- first_name: Line V
full_name: Ugelvig, Line V
id: 3DC97C8E-F248-11E8-B48F-1D18A9856A87
last_name: Ugelvig
orcid: 0000-0003-1832-8883
- first_name: Edouard
full_name: Tourdot, Edouard
last_name: Tourdot
- first_name: Jürgen
full_name: Heinze, Jürgen
last_name: Heinze
- first_name: Claudie
full_name: Doums, Claudie
last_name: Doums
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
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. Behavioral
Ecology and Sociobiology. 2014;68(10):1701-1710. doi:10.1007/s00265-014-1778-8
apa: Westhus, C., Ugelvig, L. V., 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. Springer. https://doi.org/10.1007/s00265-014-1778-8
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.” Behavioral Ecology and Sociobiology.
Springer, 2014. https://doi.org/10.1007/s00265-014-1778-8.
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,” Behavioral Ecology and Sociobiology, vol. 68, no. 10. Springer,
pp. 1701–1710, 2014.
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.” Behavioral Ecology and Sociobiology,
vol. 68, no. 10, Springer, 2014, pp. 1701–10, doi:10.1007/s00265-014-1778-8.
short: C. Westhus, L.V. Ugelvig, E. Tourdot, J. Heinze, C. Doums, S. Cremer, Behavioral
Ecology and Sociobiology 68 (2014) 1701–1710.
date_created: 2018-12-11T11:56:03Z
date_published: 2014-07-23T00:00:00Z
date_updated: 2023-02-23T14:06:46Z
day: '23'
department:
- _id: SyCr
doi: 10.1007/s00265-014-1778-8
ec_funded: 1
intvolume: ' 68'
issue: '10'
language:
- iso: eng
month: '07'
oa_version: None
page: 1701 - 1710
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '291734'
name: International IST Postdoc Fellowship Programme
- _id: 25DC711C-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '243071'
name: 'Social Vaccination in Ant Colonies: from Individual Mechanisms to Society
Effects'
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: Behavioral Ecology and Sociobiology
publication_identifier:
issn:
- 0340-5443
publication_status: published
publisher: Springer
publist_id: '4823'
quality_controlled: '1'
related_material:
record:
- id: '9742'
relation: research_data
status: public
scopus_import: '1'
status: public
title: Increased grooming after repeated brood care provides sanitary benefits in
a clonal ant
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 68
year: '2014'
...
---
_id: '2926'
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.
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"
author:
- first_name: Simon
full_name: Tragust, Simon
id: 35A7A418-F248-11E8-B48F-1D18A9856A87
last_name: Tragust
- first_name: Barbara
full_name: Mitteregger, Barbara
id: 479DDAAC-E9CD-11E9-9B5F-82450873F7A1
last_name: Mitteregger
- first_name: Vanessa
full_name: Barone, Vanessa
id: 419EECCC-F248-11E8-B48F-1D18A9856A87
last_name: Barone
orcid: 0000-0003-2676-3367
- first_name: Matthias
full_name: Konrad, Matthias
id: 46528076-F248-11E8-B48F-1D18A9856A87
last_name: Konrad
- first_name: Line V
full_name: Ugelvig, Line V
id: 3DC97C8E-F248-11E8-B48F-1D18A9856A87
last_name: Ugelvig
orcid: 0000-0003-1832-8883
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
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. Current Biology.
2013;23(1):76-82. doi:10.1016/j.cub.2012.11.034
apa: Tragust, S., Mitteregger, B., Barone, V., Konrad, M., Ugelvig, L. V., &
Cremer, S. (2013). Ants disinfect fungus-exposed brood by oral uptake and spread
of their poison. Current Biology. Cell Press. https://doi.org/10.1016/j.cub.2012.11.034
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.” Current Biology. Cell Press, 2013. https://doi.org/10.1016/j.cub.2012.11.034.
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,”
Current Biology, vol. 23, no. 1. Cell Press, pp. 76–82, 2013.
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.
mla: Tragust, Simon, et al. “Ants Disinfect Fungus-Exposed Brood by Oral Uptake
and Spread of Their Poison.” Current Biology, vol. 23, no. 1, Cell Press,
2013, pp. 76–82, doi:10.1016/j.cub.2012.11.034.
short: S. Tragust, B. Mitteregger, V. Barone, M. Konrad, L.V. Ugelvig, S. Cremer,
Current Biology 23 (2013) 76–82.
date_created: 2018-12-11T12:00:23Z
date_published: 2013-01-07T00:00:00Z
date_updated: 2023-09-07T12:05:08Z
day: '07'
department:
- _id: SyCr
- _id: CaHe
doi: 10.1016/j.cub.2012.11.034
ec_funded: 1
intvolume: ' 23'
issue: '1'
language:
- iso: eng
month: '01'
oa_version: None
page: 76 - 82
project:
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
- _id: 25DC711C-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '243071'
name: 'Social Vaccination in Ant Colonies: from Individual Mechanisms to Society
Effects'
- _id: 25DDF0F0-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '302004'
name: 'Pathogen Detectors Collective disease defence and pathogen detection abilities
in ant societies: a chemo-neuro-immunological approach'
publication: Current Biology
publication_status: published
publisher: Cell Press
publist_id: '3811'
quality_controlled: '1'
related_material:
record:
- id: '9757'
relation: research_data
status: public
- id: '961'
relation: dissertation_contains
status: public
scopus_import: 1
status: public
title: Ants disinfect fungus-exposed brood by oral uptake and spread of their poison
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 23
year: '2013'
...
---
_id: '2284'
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.'
acknowledgement: "The study was funded by the European Research Council (Marie Curie
ERG 036569) and Marie Curie IEF 302204 to LVU\r\nCC BY 2.0\r\n"
article_number: '225'
author:
- first_name: Simon
full_name: Tragust, Simon
id: 35A7A418-F248-11E8-B48F-1D18A9856A87
last_name: Tragust
- first_name: Line V
full_name: Ugelvig, 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
- first_name: Jürgen
full_name: Heinze, Jürgen
last_name: Heinze
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S. Pupal cocoons affect
sanitary brood care and limit fungal infections in ant colonies. BMC Evolutionary
Biology. 2013;13(1). doi:10.1186/1471-2148-13-225
apa: Tragust, S., Ugelvig, L. V., Chapuisat, M., Heinze, J., & Cremer, S. (2013).
Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies.
BMC Evolutionary Biology. BioMed Central. https://doi.org/10.1186/1471-2148-13-225
chicago: Tragust, Simon, Line V Ugelvig, Michel Chapuisat, Jürgen Heinze, and Sylvia
Cremer. “Pupal Cocoons Affect Sanitary Brood Care and Limit Fungal Infections
in Ant Colonies.” BMC Evolutionary Biology. BioMed Central, 2013. https://doi.org/10.1186/1471-2148-13-225.
ieee: S. Tragust, L. V. Ugelvig, M. Chapuisat, J. Heinze, and S. Cremer, “Pupal
cocoons affect sanitary brood care and limit fungal infections in ant colonies,”
BMC Evolutionary Biology, vol. 13, no. 1. BioMed Central, 2013.
ista: Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S. 2013. Pupal cocoons
affect sanitary brood care and limit fungal infections in ant colonies. BMC Evolutionary
Biology. 13(1), 225.
mla: Tragust, Simon, et al. “Pupal Cocoons Affect Sanitary Brood Care and Limit
Fungal Infections in Ant Colonies.” BMC Evolutionary Biology, vol. 13,
no. 1, 225, BioMed Central, 2013, doi:10.1186/1471-2148-13-225.
short: S. Tragust, L.V. Ugelvig, M. Chapuisat, J. Heinze, S. Cremer, BMC Evolutionary
Biology 13 (2013).
date_created: 2018-12-11T11:56:46Z
date_published: 2013-10-14T00:00:00Z
date_updated: 2023-02-23T14:07:06Z
day: '14'
ddc:
- '570'
department:
- _id: SyCr
doi: 10.1186/1471-2148-13-225
ec_funded: 1
file:
- access_level: open_access
checksum: c16ef36f2a10786a7885e19c4528d707
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:13:41Z
date_updated: 2020-07-14T12:45:37Z
file_id: '5026'
file_name: IST-2016-402-v1+1_1471-2148-13-225.pdf
file_size: 281736
relation: main_file
file_date_updated: 2020-07-14T12:45:37Z
has_accepted_license: '1'
intvolume: ' 13'
issue: '1'
language:
- iso: eng
month: '10'
oa: 1
oa_version: Published Version
project:
- _id: 25DC711C-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '243071'
name: 'Social Vaccination in Ant Colonies: from Individual Mechanisms to Society
Effects'
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
publication: BMC Evolutionary Biology
publication_status: published
publisher: BioMed Central
publist_id: '4647'
pubrep_id: '402'
quality_controlled: '1'
related_material:
record:
- id: '9753'
relation: research_data
status: public
scopus_import: 1
status: public
title: Pupal cocoons affect sanitary brood care and limit fungal infections in ant
colonies
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 13
year: '2013'
...
---
_id: '3242'
abstract:
- lang: eng
text: Due to the omnipresent risk of epidemics, insect societies have evolved sophisticated
disease defences at the individual and colony level. An intriguing yet little
understood phenomenon is that social contact to pathogen-exposed individuals reduces
susceptibility of previously naive nestmates to this pathogen. We tested whether
such social immunisation in Lasius ants against the entomopathogenic fungus Metarhizium
anisopliae is based on active upregulation of the immune system of nestmates following
contact to an infectious individual or passive protection via transfer of immune
effectors among group members—that is, active versus passive immunisation. We
found no evidence for involvement of passive immunisation via transfer of antimicrobials
among colony members. Instead, intensive allogrooming behaviour between naive
and pathogen-exposed ants before fungal conidia firmly attached to their cuticle
suggested passage of the pathogen from the exposed individuals to their nestmates.
By tracing fluorescence-labelled conidia we indeed detected frequent pathogen
transfer to the nestmates, where they caused low-level infections as revealed
by growth of small numbers of fungal colony forming units from their dissected
body content. These infections rarely led to death, but instead promoted an enhanced
ability to inhibit fungal growth and an active upregulation of immune genes involved
in antifungal defences (defensin and prophenoloxidase, PPO). Contrarily, there
was no upregulation of the gene cathepsin L, which is associated with antibacterial
and antiviral defences, and we found no increased antibacterial activity of nestmates
of fungus-exposed ants. This indicates that social immunisation after fungal exposure
is specific, similar to recent findings for individual-level immune priming in
invertebrates. Epidemiological modeling further suggests that active social immunisation
is adaptive, as it leads to faster elimination of the disease and lower death
rates than passive immunisation. Interestingly, humans have also utilised the
protective effect of low-level infections to fight smallpox by intentional transfer
of low pathogen doses (“variolation” or “inoculation”).
acknowledgement: Funding for this project was obtained by the German Research Foundation
DFG (http://www.dfg.de/en/index.jsp) as an Individual Research Grant (CR118/2-1
to SC) and the European Research Council (http://erc.europa.eu/) in form of two
ERC Starting Grants (ERC-2009-StG240371-SocialVaccines to SC and ERC-2010-StG259294-LatentCauses
to FJT). In addition, the Junge Akademie (Young Academy of the Berlin-Brandenburg
Academy of Sciences and Humanities and the National Academy of Sciences Leopoldina
(http://www.diejungeakademie.de/english/index.html) funded this joint Antnet project
of SC and FJT. The funders had no role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
article_number: e1001300
author:
- first_name: Matthias
full_name: Konrad, Matthias
id: 46528076-F248-11E8-B48F-1D18A9856A87
last_name: Konrad
- first_name: Meghan
full_name: Vyleta, Meghan
id: 418901AA-F248-11E8-B48F-1D18A9856A87
last_name: Vyleta
- first_name: Fabian
full_name: Theis, Fabian
last_name: Theis
- first_name: Miriam
full_name: Stock, Miriam
id: 42462816-F248-11E8-B48F-1D18A9856A87
last_name: Stock
- first_name: Simon
full_name: Tragust, Simon
id: 35A7A418-F248-11E8-B48F-1D18A9856A87
last_name: Tragust
- first_name: Martina
full_name: Klatt, Martina
id: E60F29C6-E9AE-11E9-AF6E-D190C7302F38
last_name: Klatt
- first_name: Verena
full_name: Drescher, Verena
last_name: Drescher
- first_name: Carsten
full_name: Marr, Carsten
last_name: Marr
- first_name: Line V
full_name: Ugelvig, Line V
id: 3DC97C8E-F248-11E8-B48F-1D18A9856A87
last_name: Ugelvig
orcid: 0000-0003-1832-8883
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Konrad M, Vyleta M, Theis F, et al. Social transfer of pathogenic fungus promotes
active immunisation in ant colonies. PLoS Biology. 2012;10(4). doi:10.1371/journal.pbio.1001300
apa: Konrad, M., Vyleta, M., Theis, F., Stock, M., Tragust, S., Klatt, M., … Cremer,
S. (2012). Social transfer of pathogenic fungus promotes active immunisation in
ant colonies. PLoS Biology. Public Library of Science. https://doi.org/10.1371/journal.pbio.1001300
chicago: Konrad, Matthias, Meghan Vyleta, Fabian Theis, Miriam Stock, Simon Tragust,
Martina Klatt, Verena Drescher, Carsten Marr, Line V Ugelvig, and Sylvia Cremer.
“Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies.”
PLoS Biology. Public Library of Science, 2012. https://doi.org/10.1371/journal.pbio.1001300.
ieee: M. Konrad et al., “Social transfer of pathogenic fungus promotes active
immunisation in ant colonies,” PLoS Biology, vol. 10, no. 4. Public Library
of Science, 2012.
ista: Konrad M, Vyleta M, Theis F, Stock M, Tragust S, Klatt M, Drescher V, Marr
C, Ugelvig LV, Cremer S. 2012. Social transfer of pathogenic fungus promotes active
immunisation in ant colonies. PLoS Biology. 10(4), e1001300.
mla: Konrad, Matthias, et al. “Social Transfer of Pathogenic Fungus Promotes Active
Immunisation in Ant Colonies.” PLoS Biology, vol. 10, no. 4, e1001300,
Public Library of Science, 2012, doi:10.1371/journal.pbio.1001300.
short: M. Konrad, M. Vyleta, F. Theis, M. Stock, S. Tragust, M. Klatt, V. Drescher,
C. Marr, L.V. Ugelvig, S. Cremer, PLoS Biology 10 (2012).
date_created: 2018-12-11T12:02:13Z
date_published: 2012-04-03T00:00:00Z
date_updated: 2023-02-23T14:07:11Z
day: '03'
ddc:
- '570'
- '579'
department:
- _id: SyCr
doi: 10.1371/journal.pbio.1001300
ec_funded: 1
file:
- access_level: open_access
checksum: 4ebacefd9fbab5c68adf829124115fd1
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:08:28Z
date_updated: 2020-07-14T12:46:04Z
file_id: '4689'
file_name: IST-2012-96-v1+1_journal.pbio.1001300.pdf
file_size: 674228
relation: main_file
file_date_updated: 2020-07-14T12:46:04Z
has_accepted_license: '1'
intvolume: ' 10'
issue: '4'
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
project:
- _id: 25DAF0B2-B435-11E9-9278-68D0E5697425
grant_number: CR-118/3-1
name: Host-Parasite Coevolution
- _id: 25DC711C-B435-11E9-9278-68D0E5697425
call_identifier: FP7
grant_number: '243071'
name: 'Social Vaccination in Ant Colonies: from Individual Mechanisms to Society
Effects'
- _id: 25E0E184-B435-11E9-9278-68D0E5697425
name: Antnet
publication: PLoS Biology
publication_status: published
publisher: Public Library of Science
publist_id: '3434'
pubrep_id: '96'
quality_controlled: '1'
related_material:
record:
- id: '9755'
relation: research_data
status: public
scopus_import: 1
status: public
title: Social transfer of pathogenic fungus promotes active immunisation in ant colonies
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 10
year: '2012'
...