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  • 1
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    eLife Sciences Publications, Ltd ; 2018
    In:  eLife Vol. 7 ( 2018-01-09)
    Details
    In: eLife, eLife Sciences Publications, Ltd, Vol. 7 ( 2018-01-09)
    Abstract: Ants live in crowded societies where disease can spread rapidly and take a heavy toll on the community. Ants have a number of ways to prevent these outbreaks before they become a problem. Like many other social species, they practice good hygiene and groom nest mates that have picked up a pathogen, which helps them to recover and to reduce the likelihood of the disease spreading. Unlike other social species, ants appear to have evolved collective disease defence, or social immunity, because their colonies behave like a ‘superorganism’, in which the society behaves much like a single organism would. Like an individual animal that has an infection, the colony needs to be able to eliminate infections collectively when a nest mate falls ill, to prevent the disease from spreading. To understand how an ant colony protects itself when the care fails and a colony member contracts a lethal infection, Pull et al. infected the brood of the invasive garden ant with a common soil fungus. Using a combination of chemical analyses and behavioural observations, it was shown that the infected pupae emitted a chemical cue, which the tending ants could detect. Using a microscopic camera, Pull et al. found that when the ants sensed the cue, they would unpack the infected pupae from their cocoons and bite them. They then sprayed them with an antiseptic poison, which entered the hole in the pupae’s body, killing both the pupae and the fungus inside, before it had a chance to spread. This process of destructive disinfection may seem like a large sacrifice, but it helps to protect the rest of the colony from a fungus that could lead to much greater damage. The tending ants were acting within the superorganism of the colony much like immune cells act within an individual’s body – honing in on infected cells and destroying them before the pathogen can spread to other cells. This suggests that the ability to detect and destroy harmful elements was necessary for both the evolution of multicellular organisms, and from single animals to superorganisms.
    Type of Medium: Online Resource
    ISSN: 2050-084X
    URL: Article
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    DOI: 10.7554/eLife.32073
    DOI: 10.7554/eLife.32073.001
    DOI: 10.7554/eLife.32073.002
    DOI: 10.7554/eLife.32073.003
    DOI: 10.7554/eLife.32073.004
    DOI: 10.7554/eLife.32073.005
    DOI: 10.7554/eLife.32073.006
    DOI: 10.7554/eLife.32073.007
    DOI: 10.7554/eLife.32073.008
    DOI: 10.7554/eLife.32073.009
    DOI: 10.7554/eLife.32073.010
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    DOI: 10.7554/eLife.32073.012
    DOI: 10.7554/eLife.32073.013
    DOI: 10.7554/eLife.32073.014
    DOI: 10.7554/eLife.32073.015
    DOI: 10.7554/eLife.32073.016
    DOI: 10.7554/eLife.32073.017
    DOI: 10.7554/eLife.32073.018
    DOI: 10.7554/eLife.32073.019
    DOI: 10.7554/eLife.32073.020
    DOI: 10.7554/eLife.32073.021
    DOI: 10.7554/eLife.32073.022
    DOI: 10.7554/eLife.32073.023
    DOI: 10.7554/eLife.32073.024
    DOI: 10.7554/eLife.32073.028
    DOI: 10.7554/eLife.32073.029
    Language: English
    Publisher: eLife Sciences Publications, Ltd
    Publication Date: 2018
    detail.hit.zdb_id: 2687154-3
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  • 2
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    Trade-offs between immunity and competitive ability in fighting ant males
    Springer Science and Business Media LLC ; 2023
    In:  BMC Ecology and Evolution Vol. 23, No. 1 ( 2023-08-07)
    Details
    In: BMC Ecology and Evolution, Springer Science and Business Media LLC, Vol. 23, No. 1 ( 2023-08-07)
    Abstract: Fighting disease while fighting rivals exposes males to constraints and trade-offs during male-male competition. We here tested how both the stage and intensity of infection with the fungal pathogen Metarhizium robertsii interfere with fighting success in Cardiocondyla obscurior ant males. Males of this species have evolved long lifespans during which they can gain many matings with the young queens of the colony, if successful in male-male competition. Since male fights occur inside the colony, the outcome of male-male competition can further be biased by interference of the colony’s worker force. Results We found that severe, but not yet mild, infection strongly impaired male fighting success. In late-stage infection, this could be attributed to worker aggression directed towards the infected rather than the healthy male and an already very high male morbidity even in the absence of fighting. Shortly after pathogen exposure, however, male mortality was particularly increased during combat. Since these males mounted a strong immune response, their reduced fighting success suggests a trade-off between immune investment and competitive ability already early in the infection. Even if the males themselves showed no difference in the number of attacks they raised against their healthy rivals across infection stages and levels, severely infected males were thus losing in male-male competition from an early stage of infection on. Conclusions Males of the ant C. obscurior have a well-developed immune system that raises a strong immune response very fast after fungal exposure. This allows them to cope with mild pathogen exposures without compromising their success in male-male competition, and hence to gain multiple mating opportunities with the emerging virgin queens of the colony. Under severe infection, however, they are weak fighters and rarely survive a combat already at early infection when raising an immune response, as well as at progressed infection, when they are morbid and preferentially targeted by worker aggression. Workers thereby remove males that pose a future disease threat by biasing male-male competition. Our study thus reveals a novel social immunity mechanism how social insect workers protect the colony against disease risk.
    Type of Medium: Online Resource
    ISSN: 2730-7182
    URL: Article
    DOI: 10.1186/s12862-023-02137-7
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2023
    detail.hit.zdb_id: 3053924-9
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  • 3
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    Social network plasticity decreases disease transmission in a eusocial insect
    American Association for the Advancement of Science (AAAS) ; 2018
    In:  Science Vol. 362, No. 6417 ( 2018-11-23), p. 941-945
    Details
    In: Science, American Association for the Advancement of Science (AAAS), Vol. 362, No. 6417 ( 2018-11-23), p. 941-945
    Abstract: Animal social networks are shaped by multiple selection pressures, including the need to ensure efficient communication and functioning while simultaneously limiting disease transmission. Social animals could potentially further reduce epidemic risk by altering their social networks in the presence of pathogens, yet there is currently no evidence for such pathogen-triggered responses. We tested this hypothesis experimentally in the ant Lasius niger using a combination of automated tracking, controlled pathogen exposure, transmission quantification, and temporally explicit simulations. Pathogen exposure induced behavioral changes in both exposed ants and their nestmates, which helped contain the disease by reinforcing key transmission-inhibitory properties of the colony’s contact network. This suggests that social network plasticity in response to pathogens is an effective strategy for mitigating the effects of disease in social groups.
    Type of Medium: Online Resource
    ISSN: 0036-8075 , 1095-9203
    URL: Article
    DOI: 10.1126/science.aat4793
    RVK:
    TA 1000
    RVK:
    WA 15000
    Language: English
    Publisher: American Association for the Advancement of Science (AAAS)
    Publication Date: 2018
    detail.hit.zdb_id: 128410-1
    detail.hit.zdb_id: 2066996-3
    detail.hit.zdb_id: 2060783-0
    SSG: 11
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  • 4
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    Ant queens increase their reproductive efforts after pathogen infection
    The Royal Society ; 2017
    In:  Royal Society Open Science Vol. 4, No. 7 ( 2017-07), p. 170547-
    Details
    In: Royal Society Open Science, The Royal Society, Vol. 4, No. 7 ( 2017-07), p. 170547-
    Abstract: Infections with potentially lethal pathogens may negatively affect an individual's lifespan and decrease its reproductive value. The terminal investment hypothesis predicts that individuals faced with a reduced survival should invest more into reproduction instead of maintenance and growth. Several studies suggest that individuals are indeed able to estimate their body condition and to increase their reproductive effort with approaching death, while other studies gave ambiguous results. We investigate whether queens of a perennial social insect (ant) are able to boost their reproduction following infection with an obligate killing pathogen. Social insect queens are special with regard to reproduction and aging, as they outlive conspecific non-reproductive workers. Moreover, in the ant Cardiocondyla obscurior , fecundity increases with queen age. However, it remained unclear whether this reflects negative reproductive senescence or terminal investment in response to approaching death. Here, we test whether queens of C. obscurior react to infection with the entomopathogenic fungus Metarhizium brunneum by an increased egg-laying rate. We show that a fungal infection triggers a reinforced investment in reproduction in queens. This adjustment of the reproductive rate by ant queens is consistent with predictions of the terminal investment hypothesis and is reported for the first time in a social insect.
    Type of Medium: Online Resource
    ISSN: 2054-5703
    URL: Article
    DOI: 10.1098/rsos.170547
    Language: English
    Publisher: The Royal Society
    Publication Date: 2017
    detail.hit.zdb_id: 2787755-3
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  • 5
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    Table_1.XLSX
    Frontiers Media SA ; 2023
    In:  Frontiers in Microbiology Vol. 14 ( 2023-3-16)
    Details
    In: Frontiers in Microbiology, Frontiers Media SA, Vol. 14 ( 2023-3-16)
    Abstract: Hosts can carry many viruses in their bodies, but not all of them cause disease. We studied ants as a social host to determine both their overall viral repertoire and the subset of actively infecting viruses across natural populations of three subfamilies: the Argentine ant ( Linepithema humile , Dolichoderinae), the invasive garden ant ( Lasius neglectus , Formicinae) and the red ant ( Myrmica rubra , Myrmicinae). We used a dual sequencing strategy to reconstruct complete virus genomes by RNA-seq and to simultaneously determine the small interfering RNAs (siRNAs) by small RNA sequencing (sRNA-seq), which constitute the host antiviral RNAi immune response. This approach led to the discovery of 41 novel viruses in ants and revealed a host ant-specific RNAi response (21 vs. 22 nt siRNAs) in the different ant species. The efficiency of the RNAi response (sRNA/RNA read count ratio) depended on the virus and the respective ant species, but not its population. Overall, we found the highest virus abundance and diversity per population in Li. humile , followed by La. neglectus and M. rubra . Argentine ants also shared a high proportion of viruses between populations, whilst overlap was nearly absent in M. rubra . Only one of the 59 viruses was found to infect two of the ant species as hosts, revealing high host-specificity in active infections. In contrast, six viruses actively infected one ant species, but were found as contaminants only in the others. Disentangling spillover of disease-causing infection from non-infecting contamination across species is providing relevant information for disease ecology and ecosystem management.
    Type of Medium: Online Resource
    ISSN: 1664-302X
    URL: Article
    URL: Article
    URL: Article
    DOI: 10.3389/fmicb.2023.1119002
    DOI: 10.3389/fmicb.2023.1119002.s001
    DOI: 10.3389/fmicb.2023.1119002.s002
    Language: Unknown
    Publisher: Frontiers Media SA
    Publication Date: 2023
    detail.hit.zdb_id: 2587354-4
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  • 6
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    Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host
    The Royal Society ; 2015
    In:  Proceedings of the Royal Society B: Biological Sciences Vol. 282, No. 1799 ( 2015-01-22), p. 20141976-
    Details
    In: Proceedings of the Royal Society B: Biological Sciences, The Royal Society, Vol. 282, No. 1799 ( 2015-01-22), p. 20141976-
    Abstract: 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.
    Type of Medium: Online Resource
    ISSN: 0962-8452 , 1471-2954
    URL: Article
    DOI: 10.1098/rspb.2014.1976
    Language: English
    Publisher: The Royal Society
    Publication Date: 2015
    detail.hit.zdb_id: 1460975-7
    SSG: 12
    SSG: 25
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  • 7
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    Social immunity modulates competition between coinfecting pathogens
    Wiley ; 2020
    In:  Ecology Letters Vol. 23, No. 3 ( 2020-03), p. 565-574
    Details
    In: Ecology Letters, Wiley, Vol. 23, No. 3 ( 2020-03), p. 565-574
    Abstract: 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.
    Type of Medium: Online Resource
    ISSN: 1461-023X , 1461-0248
    URL: Issue
    URL: Article
    DOI: 10.1111/ele.v23.3
    DOI: 10.1111/ele.13458
    Language: English
    Publisher: Wiley
    Publication Date: 2020
    detail.hit.zdb_id: 2020195-3
    SSG: 12
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  • 8
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    Dynamic pathogen detection and social feedback shape collective hygiene in ants
    Springer Science and Business Media LLC ; 2023
    In:  Nature Communications Vol. 14, No. 1 ( 2023-06-03)
    Details
    In: Nature Communications, Springer Science and Business Media LLC, Vol. 14, No. 1 ( 2023-06-03)
    Abstract: Cooperative disease defense emerges as group-level collective behavior, yet how group members make the underlying individual decisions is poorly understood. Using garden ants and fungal pathogens as an experimental model, we derive the rules governing individual ant grooming choices and show how they produce colony-level hygiene. Time-resolved behavioral analysis, pathogen quantification, and probabilistic modeling reveal that ants increase grooming and preferentially target highly-infectious individuals when perceiving high pathogen load, but transiently suppress grooming after having been groomed by nestmates. Ants thus react to both, the infectivity of others and the social feedback they receive on their own contagiousness. While inferred solely from momentary ant decisions, these behavioral rules quantitatively predict hour-long experimental dynamics, and synergistically combine into efficient colony-wide pathogen removal. Our analyses show that noisy individual decisions based on only local, incomplete, yet dynamically-updated information on pathogen threat and social feedback can lead to potent collective disease defense.
    Type of Medium: Online Resource
    ISSN: 2041-1723
    URL: Article
    DOI: 10.1038/s41467-023-38947-y
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2023
    detail.hit.zdb_id: 2553671-0
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  • 9
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    Pathogen evasion of social immunity
    Springer Science and Business Media LLC ; 2023
    In:  Nature Ecology & Evolution Vol. 7, No. 3 ( 2023-02-02), p. 450-460
    Details
    In: Nature Ecology & Evolution, Springer Science and Business Media LLC, Vol. 7, No. 3 ( 2023-02-02), p. 450-460
    Abstract: 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.
    Type of Medium: Online Resource
    ISSN: 2397-334X
    URL: Article
    DOI: 10.1038/s41559-023-01981-6
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2023
    detail.hit.zdb_id: 2879715-2
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  • 10
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    Ants avoid superinfections by performing risk-adjusted sanitary care
    Proceedings of the National Academy of Sciences ; 2018
    In:  Proceedings of the National Academy of Sciences Vol. 115, No. 11 ( 2018-03-13), p. 2782-2787
    Details
    In: Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 115, No. 11 ( 2018-03-13), p. 2782-2787
    Abstract: Being cared for when sick is a benefit of sociality that can reduce disease and improve survival of group members. However, individuals providing care risk contracting infectious diseases themselves. If they contract a low pathogen dose, they may develop low-level infections that do not cause disease but still affect host immunity by either decreasing or increasing the host’s vulnerability to subsequent infections. Caring for contagious individuals can thus significantly alter the future disease susceptibility of caregivers. Using ants and their fungal pathogens as a model system, we tested if the altered disease susceptibility of experienced caregivers, in turn, affects their expression of sanitary care behavior. We found that low-level infections contracted during sanitary care had protective or neutral effects on secondary exposure to the same (homologous) pathogen but consistently caused high mortality on superinfection with a different (heterologous) pathogen. In response to this risk, the ants selectively adjusted the expression of their sanitary care. Specifically, the ants performed less grooming and more antimicrobial disinfection when caring for nestmates contaminated with heterologous pathogens compared with homologous ones. By modulating the components of sanitary care in this way the ants acquired less infectious particles of the heterologous pathogens, resulting in reduced superinfection. The performance of risk-adjusted sanitary care reveals the remarkable capacity of ants to react to changes in their disease susceptibility, according to their own infection history and to flexibly adjust collective care to individual risk.
    Type of Medium: Online Resource
    ISSN: 0027-8424 , 1091-6490
    URL: Article
    DOI: 10.1073/pnas.1713501115
    RVK:
    TA 1000
    RVK:
    WA 15000
    Language: English
    Publisher: Proceedings of the National Academy of Sciences
    Publication Date: 2018
    detail.hit.zdb_id: 209104-5
    detail.hit.zdb_id: 1461794-8
    SSG: 11
    SSG: 12
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