TY - JOUR AB - Entire chromosomes are typically only transmitted vertically from one generation to the next. The horizontal transfer of such chromosomes has long been considered improbable, yet gained recent support in several pathogenic fungi where it may affect the fitness or host specificity. To date, it is unknown how these transfers occur, how common they are and whether they can occur between different species. In this study, we show multiple independent instances of horizontal transfers of the same accessory chromosome between two distinct strains of the asexual entomopathogenic fungusMetarhizium robertsiiduring experimental co-infection of its insect host, the Argentine ant. Notably, only the one chromosome – but no other – was transferred from the donor to the recipient strain. The recipient strain, now harboring the accessory chromosome, exhibited a competitive advantage under certain host conditions. By phylogenetic analysis we further demonstrate that the same accessory chromosome was horizontally transferred in a natural environment betweenM. robertsiiand another congeneric insect pathogen,M. guizhouense. Hence horizontal chromosome transfer is not limited to the observed frequent events within species during experimental infections but also occurs naturally across species. The transferred accessory chromosome contains genes that might be involved in its preferential horizontal transfer, encoding putative histones and histone-modifying enzymes, but also putative virulence factors that may support its establishment. Our study reveals that both intra- and interspecies horizontal transfer of entire chromosomes is more frequent than previously assumed, likely representing a not uncommon mechanism for gene exchange.Significance StatementThe enormous success of bacterial pathogens has been attributed to their ability to exchange genetic material between one another. Similarly, in eukaryotes, horizontal transfer of genetic material allowed the spread of virulence factors across species. The horizontal transfer of whole chromosomes could be an important pathway for such exchange of genetic material, but little is known about the origin of transferable chromosomes and how frequently they are exchanged. Here, we show that the transfer of accessory chromosomes - chromosomes that are non-essential but may provide fitness benefits - is common during fungal co-infections and is even possible between distant pathogenic species, highlighting the importance of horizontal gene transfer via chromosome transfer also for the evolution and function of eukaryotic pathogens. AU - Habig, Michael AU - Grasse, Anna V AU - Müller, Judith AU - Stukenbrock, Eva H. AU - Leitner, Hanna AU - Cremer, Sylvia ID - 14478 IS - 11 JF - Proceedings of the National Academy of Sciences of the United States of America SN - 0027-8424 TI - Frequent horizontal chromosome transfer between asexual fungal insect pathogens VL - 121 ER - TY - JOUR AB - 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. AU - Viljakainen, Lumi AU - Fürst, Matthias AU - Grasse, Anna V AU - Jurvansuu, Jaana AU - Oh, Jinook AU - Tolonen, Lassi AU - Eder, Thomas AU - Rattei, Thomas AU - Cremer, Sylvia ID - 12469 JF - Frontiers in Microbiology TI - Antiviral immune response reveals host-specific virus infections in natural ant populations VL - 14 ER - TY - JOUR AB - 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. AU - Casillas Perez, Barbara E AU - Bod'Ová, Katarína AU - Grasse, Anna V AU - Tkačik, Gašper AU - Cremer, Sylvia ID - 13127 JF - Nature Communications TI - Dynamic pathogen detection and social feedback shape collective hygiene in ants VL - 14 ER - TY - JOUR AB - 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. AU - Stock, Miriam AU - Milutinovic, Barbara AU - Hönigsberger, Michaela AU - Grasse, Anna V AU - Wiesenhofer, Florian AU - Kampleitner, Niklas AU - Narasimhan, Madhumitha AU - Schmitt, Thomas AU - Cremer, Sylvia ID - 12543 JF - Nature Ecology and Evolution TI - Pathogen evasion of social immunity VL - 7 ER - TY - JOUR AB - Background: Fighting disease while fighting rivals exposes males to constraints and tradeoffs during male-male competition. We here tested how both the stage and intensity of infection with the fungal pathogen Metarhizium robertsii interfered 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 evolved high immune investment, triggering an effective immune response very fast after fungal exposure. This allows them to cope with mild pathogen exposures without cost to 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 revealed a novel social immunity mechanism how social insect workers protect the colony against disease risk. AU - Metzler, Sina AU - Kirchner, Jessica AU - Grasse, Anna V AU - Cremer, Sylvia ID - 12696 JF - BMC Ecology and Evolution SN - 2730-7182 TI - Trade-offs between immunity and competitive ability in fighting ant males VL - 23 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 - 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. AU - Pull, Christopher AU - Ugelvig, Line V AU - Wiesenhofer, Florian AU - Grasse, Anna V AU - Tragust, Simon AU - Schmitt, Thomas AU - Brown, Mark AU - Cremer, Sylvia ID - 616 JF - eLife TI - Destructive disinfection of infected brood prevents systemic disease spread in ant colonies VL - 7 ER - TY - JOUR AB - 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. AU - Stroeymeyt, Nathalie AU - Grasse, Anna V AU - Crespi, Alessandro AU - Mersch, Danielle AU - Cremer, Sylvia AU - Keller, Laurent ID - 7 IS - 6417 JF - Science SN - 1095-9203 TI - Social network plasticity decreases disease transmission in a eusocial insect VL - 362 ER - TY - GEN AB - Dataset for manuscript 'Social network plasticity decreases disease transmission in a eusocial insect' Compared to previous versions: - raw image files added - correction of URLs within README.txt file AU - Stroeymeyt, Nathalie AU - Grasse, Anna V AU - Crespi, Alessandro AU - Mersch, Danielle AU - Cremer, Sylvia AU - Keller, Laurent ID - 13055 TI - Social network plasticity decreases disease transmission in a eusocial insect ER - TY - JOUR AB - 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. AU - Giehr, Julia AU - Grasse, Anna V AU - Cremer, Sylvia AU - Heinze, Jürgen AU - Schrempf, Alexandra ID - 914 IS - 7 JF - Royal Society Open Science SN - 20545703 TI - Ant queens increase their reproductive efforts after pathogen infection VL - 4 ER - TY - GEN AB - Egg laying rates and infection loads of C. obscurior queens AU - Giehr, Julia AU - Grasse, Anna V AU - Cremer, Sylvia AU - Heinze, Jürgen AU - Schrempf, Alexandra ID - 9853 TI - Raw data from ant queens increase their reproductive efforts after pathogen infection ER - TY - JOUR AB - 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. AU - Konrad, Matthias AU - Grasse, Anna V AU - Tragust, Simon AU - Cremer, Sylvia ID - 1993 IS - 1799 JF - Proceedings of the Royal Society of London Series B Biological Sciences SN - 0962-8452 TI - Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host VL - 282 ER - TY - JOUR AB - The unprecedented polymorphism in the major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection from parasites. However, do parasites also drive divergence at MHC loci between host populations, or do the effects of balancing selection maintain similarities among populations? We examined MHC variation in populations of the livebearing fish Poecilia mexicana and characterized their parasite communities. Poecilia mexicana populations in the Cueva del Azufre system are locally adapted to darkness and the presence of toxic hydrogen sulphide, representing highly divergent ecotypes or incipient species. Parasite communities differed significantly across populations, and populations with higher parasite loads had higher levels of diversity at class II MHC genes. However, despite different parasite communities, marked divergence in adaptive traits and in neutral genetic markers, we found MHC alleles to be remarkably similar among host populations. Our findings indicate that balancing selection from parasites maintains immunogenetic diversity of hosts, but this process does not promote MHC divergence in this system. On the contrary, we suggest that balancing selection on immunogenetic loci may outweigh divergent selection causing divergence, thereby hindering host divergence and speciation. Our findings support the hypothesis that balancing selection maintains MHC similarities among lineages during and after speciation (trans-species evolution). AU - Tobler, Michael AU - Plath, Martin AU - Riesch, Rüdiger AU - Schlupp, Ingo AU - Grasse, Anna V AU - Munimanda, Gopi AU - Setzer, C AU - Penn, Dustin AU - Moodley, Yoshan ID - 1905 IS - 5 JF - Journal of Evolutionary Biology SN - 1010-061X TI - Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations VL - 27 ER - TY - GEN AB - 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. AU - Konrad, Matthias AU - Grasse, Anna V AU - Tragust, Simon AU - Cremer, Sylvia ID - 9740 TI - Data from: Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host ER -