---
_id: '1830'
abstract:
- lang: eng
text: To prevent epidemics, insect societies have evolved collective disease defences
that are highly effective at curing exposed individuals and limiting disease transmission
to healthy group members. Grooming is an important sanitary behaviour—either performed
towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious
agents from the body surface of exposed individuals, but at the risk of disease
contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal
pathogen Metarhizium as a model system to study how pathogen presence affects
self-grooming and allogrooming between exposed and healthy individuals. We develop
an epidemiological SIS model to explore how experimentally observed grooming patterns
affect disease spread within the colony, thereby providing a direct link between
the expression and direction of sanitary behaviours, and their effects on colony-level
epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously
decreasing allogrooming. This behavioural modulation seems universally adaptive
and is predicted to contain disease spread in a great variety of host–pathogen
systems. In contrast, allogrooming directed towards pathogen-exposed individuals
might both increase and decrease disease risk. Our model reveals that the effect
of allogrooming depends on the balance between pathogen infectiousness and efficiency
of social host defences, which are likely to vary across host–pathogen systems.
acknowledgement: We thank Meghan L. Vyleta for the genetical fungal strain characterization
and Eva Sixt for ant drawings, Matthias Konrad for discussion and Christopher D.
Pull, Barbara Casillas-Peréz, Sebastian Novak, as well as three anonymous reviewers
and the theme issue editors Peter Kappeler and Charlie Nunn for valuable comments
on the manuscript.
article_processing_charge: No
article_type: original
author:
- first_name: Fabian
full_name: Theis, Fabian
last_name: Theis
- 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: Carsten
full_name: Marr, Carsten
last_name: Marr
- first_name: Sylvia
full_name: Cremer, Sylvia
id: 2F64EC8C-F248-11E8-B48F-1D18A9856A87
last_name: Cremer
orcid: 0000-0002-2193-3868
citation:
ama: Theis F, Ugelvig LV, Marr C, Cremer S. Opposing effects of allogrooming on
disease transmission in ant societies. Philosophical Transactions of the Royal
Society of London Series B, Biological Sciences. 2015;370(1669). doi:10.1098/rstb.2014.0108
apa: Theis, F., Ugelvig, L. V., Marr, C., & Cremer, S. (2015). Opposing effects
of allogrooming on disease transmission in ant societies. Philosophical Transactions
of the Royal Society of London. Series B, Biological Sciences. Royal Society,
The. https://doi.org/10.1098/rstb.2014.0108
chicago: Theis, Fabian, Line V Ugelvig, Carsten Marr, and Sylvia Cremer. “Opposing
Effects of Allogrooming on Disease Transmission in Ant Societies.” Philosophical
Transactions of the Royal Society of London. Series B, Biological Sciences.
Royal Society, The, 2015. https://doi.org/10.1098/rstb.2014.0108.
ieee: F. Theis, L. V. Ugelvig, C. Marr, and S. Cremer, “Opposing effects of allogrooming
on disease transmission in ant societies,” Philosophical Transactions of the
Royal Society of London. Series B, Biological Sciences, vol. 370, no. 1669.
Royal Society, The, 2015.
ista: Theis F, Ugelvig LV, Marr C, Cremer S. 2015. Opposing effects of allogrooming
on disease transmission in ant societies. Philosophical Transactions of the Royal
Society of London. Series B, Biological Sciences. 370(1669).
mla: Theis, Fabian, et al. “Opposing Effects of Allogrooming on Disease Transmission
in Ant Societies.” Philosophical Transactions of the Royal Society of London.
Series B, Biological Sciences, vol. 370, no. 1669, Royal Society, The, 2015,
doi:10.1098/rstb.2014.0108.
short: F. Theis, L.V. Ugelvig, C. Marr, S. Cremer, Philosophical Transactions of
the Royal Society of London. Series B, Biological Sciences 370 (2015).
date_created: 2018-12-11T11:54:15Z
date_published: 2015-05-26T00:00:00Z
date_updated: 2023-02-23T14:06:12Z
day: '26'
department:
- _id: SyCr
doi: 10.1098/rstb.2014.0108
ec_funded: 1
external_id:
pmid:
- '25870394'
intvolume: ' 370'
issue: '1669'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4410374/
month: '05'
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: 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'
- _id: 25E0E184-B435-11E9-9278-68D0E5697425
name: Antnet
- _id: 25E24DB2-B435-11E9-9278-68D0E5697425
name: Fellowship of Wissenschaftskolleg zu Berlin
publication: Philosophical Transactions of the Royal Society of London. Series B,
Biological Sciences
publication_identifier:
eissn:
- 1471-2970
issn:
- 0962-8436
publication_status: published
publisher: Royal Society, The
publist_id: '5273'
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title: Opposing effects of allogrooming on disease transmission in ant societies
type: journal_article
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
volume: 370
year: '2015'
...
---
_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:
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checksum: 4ebacefd9fbab5c68adf829124115fd1
content_type: application/pdf
creator: system
date_created: 2018-12-12T10:08:28Z
date_updated: 2020-07-14T12:46:04Z
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file_name: IST-2012-96-v1+1_journal.pbio.1001300.pdf
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has_accepted_license: '1'
intvolume: ' 10'
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language:
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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'
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quality_controlled: '1'
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scopus_import: 1
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title: Social transfer of pathogenic fungus promotes active immunisation in ant colonies
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legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
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...