TY - JOUR AB - Infections early in life can have enduring effects on an organism's development and immunity. In this study, we show that this equally applies to developing ‘superorganisms’––incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colonies grew more slowly than controls before winter, but reached similar sizes afterwards. Independent of exposure, queen hibernation survival improved when the ratio of pupae to workers was small. Queens that reared fewer pupae before worker emergence exhibited lower pathogen levels, indicating that high brood rearing efforts interfere with the ability of the queen's immune system to suppress pathogen proliferation. Early-life queen pathogen exposure also improved the immunocompetence of her worker offspring, as demonstrated by challenging the workers to the same pathogen a year later. Transgenerational transfer of the queen's pathogen experience to her workforce can hence durably reduce the disease susceptibility of the whole superorganism. AU - Casillas Perez, Barbara E AU - Pull, Christopher AU - Naiser, Filip AU - Naderlinger, Elisabeth AU - Matas, Jiri AU - Cremer, Sylvia ID - 10284 IS - 1 JF - Ecology Letters SN - 1461-023X TI - Early queen infection shapes developmental dynamics and induces long-term disease protection in incipient ant colonies VL - 25 ER - TY - JOUR AB - 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. AU - Milutinovic, Barbara AU - Stock, Miriam AU - Grasse, Anna V AU - Naderlinger, Elisabeth AU - Hilbe, Christian AU - Cremer, Sylvia ID - 7343 IS - 3 JF - Ecology Letters SN - 1461-023X TI - Social immunity modulates competition between coinfecting pathogens VL - 23 ER - TY - GEN AB - Coinfections with multiple pathogens can result in complex within-host dynamics affecting virulence and transmission. Whilst 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 defenses 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, whilst simultaneously increasing co-sporulation on individual cadavers and maintaining a higher pathogen diversity at the community-level. Mathematical modeling 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- and population-level. AU - Milutinovic, Barbara AU - Stock, Miriam AU - Grasse, Anna V AU - Naderlinger, Elisabeth AU - Hilbe, Christian AU - Cremer, Sylvia ID - 13060 TI - Social immunity modulates competition between coinfecting pathogens ER - TY - JOUR AB - 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. AU - Konrad, Matthias AU - Pull, Christopher AU - Metzler, Sina AU - Seif, Katharina AU - Naderlinger, Elisabeth AU - Grasse, Anna V AU - Cremer, Sylvia ID - 413 IS - 11 JF - PNAS TI - Ants avoid superinfections by performing risk-adjusted sanitary care VL - 115 ER - TY - JOUR AB - Many animals use antimicrobials to prevent or cure disease [1,2]. For example, some animals will ingest plants with medicinal properties, both prophylactically to prevent infection and therapeutically to self-medicate when sick. Antimicrobial substances are also used as topical disinfectants, to prevent infection, protect offspring and to sanitise their surroundings [1,2]. Social insects (ants, bees, wasps and termites) build nests in environments with a high abundance and diversity of pathogenic microorganisms — such as soil and rotting wood — and colonies are often densely crowded, creating conditions that favour disease outbreaks. Consequently, social insects have evolved collective disease defences to protect their colonies from epidemics. These traits can be seen as functionally analogous to the immune system of individual organisms [3,4]. This ‘social immunity’ utilises antimicrobials to prevent and eradicate infections, and to keep the brood and nest clean. However, these antimicrobial compounds can be harmful to the insects themselves, and it is unknown how colonies prevent collateral damage when using them. Here, we demonstrate that antimicrobial acids, produced by workers to disinfect the colony, are harmful to the delicate pupal brood stage, but that the pupae are protected from the acids by the presence of a silk cocoon. Garden ants spray their nests with an antimicrobial poison to sanitize contaminated nestmates and brood. Here, Pull et al show that they also prophylactically sanitise their colonies, and that the silk cocoon serves as a barrier to protect developing pupae, thus preventing collateral damage during nest sanitation. AU - Pull, Christopher AU - Metzler, Sina AU - Naderlinger, Elisabeth AU - Cremer, Sylvia ID - 55 IS - 19 JF - Current Biology TI - Protection against the lethal side effects of social immunity in ants VL - 28 ER -