---
_id: '616'
abstract:
- lang: eng
text: Social insects protect their colonies from infectious disease through collective
defences that result in social immunity. In ants, workers first try to prevent
infection of colony members. Here, we show that if this fails and a pathogen establishes
an infection, ants employ an efficient multicomponent behaviour − "destructive
disinfection" − to prevent further spread of disease through the colony.
Ants specifically target infected pupae during the pathogen's non-contagious incubation
period, relying on chemical 'sickness cues' emitted by pupae. They then remove
the pupal cocoon, perforate its cuticle and administer antimicrobial poison, which
enters the body and prevents pathogen replication from the inside out. Like the
immune system of a body that specifically targets and eliminates infected cells,
this social immunity measure sacrifices infected brood to stop the pathogen completing
its lifecycle, thus protecting the rest of the colony. Hence, the same principles
of disease defence apply at different levels of biological organisation.
article_number: e32073
article_processing_charge: Yes
author:
- first_name: Christopher
full_name: Pull, Christopher
id: 3C7F4840-F248-11E8-B48F-1D18A9856A87
last_name: Pull
orcid: 0000-0003-1122-3982
- 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: Florian
full_name: Wiesenhofer, Florian
id: 39523C54-F248-11E8-B48F-1D18A9856A87
last_name: Wiesenhofer
- 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: Thomas
full_name: Schmitt, Thomas
last_name: Schmitt
- first_name: Mark
full_name: Brown, Mark
last_name: Brown
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Pull C, Ugelvig LV, Wiesenhofer F, et al. Destructive disinfection of infected
brood prevents systemic disease spread in ant colonies. eLife. 2018;7.
doi:10.7554/eLife.32073
apa: Pull, C., Ugelvig, L. V., Wiesenhofer, F., Grasse, A. V., Tragust, S., Schmitt,
T., … Cremer, S. (2018). Destructive disinfection of infected brood prevents systemic
disease spread in ant colonies. ELife. eLife Sciences Publications. https://doi.org/10.7554/eLife.32073
chicago: Pull, Christopher, Line V Ugelvig, Florian Wiesenhofer, Anna V Grasse,
Simon Tragust, Thomas Schmitt, Mark Brown, and Sylvia Cremer. “Destructive Disinfection
of Infected Brood Prevents Systemic Disease Spread in Ant Colonies.” ELife.
eLife Sciences Publications, 2018. https://doi.org/10.7554/eLife.32073.
ieee: C. Pull et al., “Destructive disinfection of infected brood prevents
systemic disease spread in ant colonies,” eLife, vol. 7. eLife Sciences
Publications, 2018.
ista: Pull C, Ugelvig LV, Wiesenhofer F, Grasse AV, Tragust S, Schmitt T, Brown
M, Cremer S. 2018. Destructive disinfection of infected brood prevents systemic
disease spread in ant colonies. eLife. 7, e32073.
mla: Pull, Christopher, et al. “Destructive Disinfection of Infected Brood Prevents
Systemic Disease Spread in Ant Colonies.” ELife, vol. 7, e32073, eLife
Sciences Publications, 2018, doi:10.7554/eLife.32073.
short: C. Pull, L.V. Ugelvig, F. Wiesenhofer, A.V. Grasse, S. Tragust, T. Schmitt,
M. Brown, S. Cremer, ELife 7 (2018).
date_created: 2018-12-11T11:47:31Z
date_published: 2018-01-09T00:00:00Z
date_updated: 2023-09-11T12:54:26Z
day: '09'
ddc:
- '570'
- '590'
department:
- _id: SyCr
doi: 10.7554/eLife.32073
ec_funded: 1
external_id:
isi:
- '000419601300001'
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creator: system
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date_updated: 2020-07-14T12:47:20Z
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file_name: IST-2018-978-v1+1_elife-32073-v1.pdf
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month: '01'
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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: 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: eLife
publication_status: published
publisher: eLife Sciences Publications
publist_id: '7188'
pubrep_id: '978'
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scopus_import: '1'
status: public
title: Destructive disinfection of infected brood prevents systemic disease spread
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: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 7
year: '2018'
...
---
_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: '9740'
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.
article_processing_charge: No
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. Data from: Anti-pathogen protection
versus survival costs mediated by an ectosymbiont in an ant host. 2014. doi:10.5061/dryad.vm0vc'
apa: 'Konrad, M., Grasse, A. V., Tragust, S., & Cremer, S. (2014). Data from:
Anti-pathogen protection versus survival costs mediated by an ectosymbiont in
an ant host. Dryad. https://doi.org/10.5061/dryad.vm0vc'
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. https://doi.org/10.5061/dryad.vm0vc.'
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,
10.5061/dryad.vm0vc.'
mla: 'Konrad, Matthias, et al. Data from: Anti-Pathogen Protection versus Survival
Costs Mediated by an Ectosymbiont in an Ant Host. Dryad, 2014, doi:10.5061/dryad.vm0vc.'
short: M. Konrad, A.V. Grasse, S. Tragust, S. Cremer, (2014).
date_created: 2021-07-28T08:38:40Z
date_published: 2014-11-13T00:00:00Z
date_updated: 2023-02-23T10:23:32Z
day: '13'
department:
- _id: SyCr
doi: 10.5061/dryad.vm0vc
main_file_link:
- open_access: '1'
url: https://doi.org/10.5061/dryad.vm0vc
month: '11'
oa: 1
oa_version: Published Version
publisher: Dryad
related_material:
record:
- id: '1993'
relation: used_in_publication
status: public
status: public
title: 'Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont
in an ant host'
type: research_data_reference
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
year: '2014'
...
---
_id: '9753'
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.'
article_processing_charge: No
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. Data from: Pupal cocoons
affect sanitary brood care and limit fungal infections in ant colonies. 2014.
doi:10.5061/dryad.nc0gc'
apa: 'Tragust, S., Ugelvig, L. V., Chapuisat, M., Heinze, J., & Cremer, S. (2014).
Data from: Pupal cocoons affect sanitary brood care and limit fungal infections
in ant colonies. Dryad. https://doi.org/10.5061/dryad.nc0gc'
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. https://doi.org/10.5061/dryad.nc0gc.'
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.'
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, 10.5061/dryad.nc0gc.'
mla: 'Tragust, Simon, et al. Data from: Pupal Cocoons Affect Sanitary Brood Care
and Limit Fungal Infections in Ant Colonies. Dryad, 2014, doi:10.5061/dryad.nc0gc.'
short: S. Tragust, L.V. Ugelvig, M. Chapuisat, J. Heinze, S. Cremer, (2014).
date_created: 2021-07-30T08:24:11Z
date_published: 2014-10-08T00:00:00Z
date_updated: 2023-02-23T10:36:17Z
day: '08'
department:
- _id: SyCr
doi: 10.5061/dryad.nc0gc
main_file_link:
- open_access: '1'
url: https://doi.org/10.5061/dryad.nc0gc
month: '10'
oa: 1
oa_version: Published Version
publisher: Dryad
related_material:
record:
- id: '2284'
relation: used_in_publication
status: public
status: public
title: 'Data from: Pupal cocoons affect sanitary brood care and limit fungal infections
in ant colonies'
type: research_data_reference
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
year: '2014'
...
---
_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
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title: Pupal cocoons affect sanitary brood care and limit fungal infections in ant
colonies
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abstract:
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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
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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: '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'
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title: Social transfer of pathogenic fungus promotes active immunisation in ant colonies
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text: To fight infectious diseases, host immune defences are employed at multiple
levels. Sanitary behaviour, such as pathogen avoidance and removal, acts as a
first line of defence 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 towards pathogen-exposed group members [2].
One of the most common behaviours 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 as 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
behaviour extends current understanding of grooming and the establishment of social
immunity in insect societies.
article_processing_charge: No
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. Data from:
Ants disinfect fungus-exposed brood by oral uptake and spread of their poison.
2012. doi:10.5061/dryad.61649'
apa: 'Tragust, S., Mitteregger, B., Barone, V., Konrad, M., Ugelvig, L. V., &
Cremer, S. (2012). Data from: Ants disinfect fungus-exposed brood by oral uptake
and spread of their poison. Dryad. https://doi.org/10.5061/dryad.61649'
chicago: 'Tragust, Simon, Barbara Mitteregger, Vanessa Barone, Matthias Konrad,
Line V Ugelvig, and Sylvia Cremer. “Data from: Ants Disinfect Fungus-Exposed Brood
by Oral Uptake and Spread of Their Poison.” Dryad, 2012. https://doi.org/10.5061/dryad.61649.'
ieee: 'S. Tragust, B. Mitteregger, V. Barone, M. Konrad, L. V. Ugelvig, and S. Cremer,
“Data from: Ants disinfect fungus-exposed brood by oral uptake and spread of their
poison.” Dryad, 2012.'
ista: 'Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. 2012.
Data from: Ants disinfect fungus-exposed brood by oral uptake and spread of their
poison, Dryad, 10.5061/dryad.61649.'
mla: 'Tragust, Simon, et al. Data from: Ants Disinfect Fungus-Exposed Brood by
Oral Uptake and Spread of Their Poison. Dryad, 2012, doi:10.5061/dryad.61649.'
short: S. Tragust, B. Mitteregger, V. Barone, M. Konrad, L.V. Ugelvig, S. Cremer,
(2012).
date_created: 2021-07-30T12:31:31Z
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