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 - Hosts can alter their strategy towards pathogens during their lifetime; that is, they can show phenotypic plasticity in immunity or life history. Immune priming is one such example, where a previous encounter with a pathogen confers enhanced protection upon secondary challenge, resulting in reduced pathogen load (i.e., resistance) and improved host survival. However, an initial encounter might also enhance tolerance, particularly to less virulent opportunistic pathogens that establish persistent infections. In this scenario, individuals are better able to reduce the negative fecundity consequences that result from a high pathogen burden. Finally, previous exposure may also lead to life‐history adjustments, such as terminal investment into reproduction. Using different Drosophila melanogaster host genotypes and two bacterial pathogens, Lactococcus lactis and Pseudomonas entomophila, we tested whether previous exposure results in resistance or tolerance and whether it modifies immune gene expression during an acute‐phase infection (one day post‐challenge). We then asked whether previous pathogen exposure affects chronic‐phase pathogen persistence and longer‐term survival (28 days post‐challenge). We predicted that previous exposure would increase host resistance to an early stage bacterial infection while it might come at a cost to host fecundity tolerance. We reasoned that resistance would be due in part to stronger immune gene expression after challenge. We expected that previous exposure would improve long‐term survival, that it would reduce infection persistence, and we expected to find genetic variation in these responses. We found that previous exposure to P. entomophila weakened host resistance to a second infection independent of genotype and had no effect on immune gene expression. Fecundity tolerance showed genotypic variation but was not influenced by previous exposure. However, L. lactis persisted as a chronic infection, whereas survivors cleared the more pathogenic P. entomophila infection. To our knowledge, this is the first study that addresses host tolerance to bacteria in relation to previous exposure, taking a multi‐faceted approach to address the topic. Our results suggest that previous exposure comes with transient costs to resistance during the early stage of infection in this host–pathogen system and that infection persistence may be bacterium‐specific. AU - Kutzer, Megan AU - Kurtz, Joachim AU - Armitage, Sophie A.O. ID - 6105 IS - 4 JF - Journal of Animal Ecology SN - 00218790 TI - A multi-faceted approach testing the effects of previous bacterial exposure on resistance and tolerance VL - 88 ER - TY - GEN AB - 1. Hosts can alter their strategy towards pathogens during their lifetime, i.e., they can show phenotypic plasticity in immunity or life history. Immune priming is one such example, where a previous encounter with a pathogen confers enhanced protection upon secondary challenge, resulting in reduced pathogen load (i.e. resistance) and improved host survival. However, an initial encounter might also enhance tolerance, particularly to less virulent opportunistic pathogens that establish persistent infections. In this scenario, individuals are better able to reduce the negative fitness consequences that result from a high pathogen load. Finally, previous exposure may also lead to life history adjustments, such as terminal investment into reproduction. 2. Using different Drosophila melanogaster host genotypes and two bacterial pathogens, Lactococcus lactis and Pseudomonas entomophila, we tested if previous exposure results in resistance or tolerance and whether it modifies immune gene expression during an acute-phase infection (one day post-challenge). We then asked if previous pathogen exposure affects chronic-phase pathogen persistence and longer-term survival (28 days post-challenge). 3. We predicted that previous exposure would increase host resistance to an early stage bacterial infection while it might come at a cost to host fecundity tolerance. We reasoned that resistance would be due in part to stronger immune gene expression after challenge. We expected that previous exposure would improve long-term survival, that it would reduce infection persistence, and we expected to find genetic variation in these responses. 4. We found that previous exposure to P. entomophila weakened host resistance to a second infection independent of genotype and had no effect on immune gene expression. Fecundity tolerance showed genotypic variation but was not influenced by previous exposure. However, L. lactis persisted as a chronic infection, whereas survivors cleared the more pathogenic P. entomophila infection. 5. To our knowledge, this is the first study that addresses host tolerance to bacteria in relation to previous exposure, taking a multi-faceted approach to address the topic. Our results suggest that previous exposure comes with transient costs to resistance during the early stage of infection in this host-pathogen system and that infection persistence may be bacterium-specific. AU - Kutzer, Megan AU - Kurtz, Joachim AU - Armitage, Sophie A.O. ID - 9806 TI - Data from: A multi-faceted approach testing the effects of previous bacterial exposure on resistance and tolerance ER - TY - JOUR AB - Ant invasions are often harmful to native species communities. Their pathogens and host disease defense mechanisms may be one component of their devastating success. First, they can introduce harmful diseases to their competitors in the introduced range, to which they themselves are tolerant. Second, their supercolonial social structure of huge multi-queen nest networks means that they will harbor a broad pathogen spectrum and high pathogen load while remaining resilient, unlike the smaller, territorial colonies of the native species. Thus, it is likely that invasive ants act as a disease reservoir, promoting their competitive advantage and invasive success. AU - Cremer, Sylvia ID - 6415 JF - Current Opinion in Insect Science SN - 22145745 TI - Pathogens and disease defense of invasive ants VL - 33 ER - TY - JOUR AB - When animals become sick, infected cells and an armada of activated immune cells attempt to eliminate the pathogen from the body. Once infectious particles have breached the body's physical barriers of the skin or gut lining, an initially local response quickly escalates into a systemic response, attracting mobile immune cells to the site of infection. These cells complement the initial, unspecific defense with a more specialized, targeted response. This can also provide long-term immune memory and protection against future infection. The cell-autonomous defenses of the infected cells are thus aided by the actions of recruited immune cells. These specialized cells are the most mobile cells in the body, constantly patrolling through the otherwise static tissue to detect incoming pathogens. Such constant immune surveillance means infections are noticed immediately and can be rapidly cleared from the body. Some immune cells also remove infected cells that have succumbed to infection. All this prevents pathogen replication and spread to healthy tissues. Although this may involve the sacrifice of some somatic tissue, this is typically replaced quickly. Particular care is, however, given to the reproductive organs, which should always remain disease free (immune privilege). AU - Cremer, Sylvia ID - 6552 IS - 11 JF - Current Biology SN - 09609822 TI - Social immunity in insects VL - 29 ER - TY - CHAP AB - Social insects (i.e., ants, termites and the social bees and wasps) protect their colonies from disease using a combination of individual immunity and collectively performed defenses, termed social immunity. The first line of social immune defense is sanitary care, which is performed by colony members to protect their pathogen-exposed nestmates from developing an infection. If sanitary care fails and an infection becomes established, a second line of social immune defense is deployed to stop disease transmission within the colony and to protect the valuable queens, which together with the males are the reproductive individuals of the colony. Insect colonies are separated into these reproductive individuals and the sterile worker force, forming a superorganismal reproductive unit reminiscent of the differentiated germline and soma in a multicellular organism. Ultimately, the social immune response preserves the germline of the superorganism insect colony and increases overall fitness of the colony in case of disease. AU - Cremer, Sylvia AU - Kutzer, Megan ED - Choe, Jae ID - 7513 SN - 9780128132517 T2 - Encyclopedia of Animal Behavior TI - Social immunity ER - TY - THES AB - Social insect colonies tend to have numerous members which function together like a single organism in such harmony that the term ``super-organism'' is often used. In this analogy the reproductive caste is analogous to the primordial germ cells of a metazoan, while the sterile worker caste corresponds to somatic cells. The worker castes, like tissues, are in charge of all functions of a living being, besides reproduction. The establishment of new super-organismal units (i.e. new colonies) is accomplished by the co-dependent castes. The term oftentimes goes beyond a metaphor. We invoke it when we speak about the metabolic rate, thermoregulation, nutrient regulation and gas exchange of a social insect colony. Furthermore, we assert that the super-organism has an immune system, and benefits from ``social immunity''. Social immunity was first summoned by evolutionary biologists to resolve the apparent discrepancy between the expected high frequency of disease outbreak amongst numerous, closely related tightly-interacting hosts, living in stable and microbially-rich environments, against the exceptionally scarce epidemic accounts in natural populations. Social immunity comprises a multi-layer assembly of behaviours which have evolved to effectively keep the pathogenic enemies of a colony at bay. The field of social immunity has drawn interest, as it becomes increasingly urgent to stop the collapse of pollinator species and curb the growth of invasive pests. In the past decade, several mechanisms of social immune responses have been dissected, but many more questions remain open. I present my work in two experimental chapters. In the first, I use invasive garden ants (*Lasius neglectus*) to study how pathogen load and its distribution among nestmates affect the grooming response of the group. Any given group of ants will carry out the same total grooming work, but will direct their grooming effort towards individuals carrying a relatively higher spore load. Contrary to expectation, the highest risk of transmission does not stem from grooming highly contaminated ants, but instead, we suggest that the grooming response likely minimizes spore loss to the environment, reducing contamination from inadvertent pickup from the substrate. The second is a comparative developmental approach. I follow black garden ant queens (*Lasius niger*) and their colonies from mating flight, through hibernation for a year. Colonies which grow fast from the start, have a lower chance of survival through hibernation, and those which survive grow at a lower pace later. This is true for colonies of naive and challenged queens. Early pathogen exposure of the queens changes colony dynamics in an unexpected way: colonies from exposed queens are more likely to grow slowly and recover in numbers only after they survive hibernation. In addition to the two experimental chapters, this thesis includes a co-authored published review on organisational immunity, where we enlist the experimental evidence and theoretical framework on which this hypothesis is built, identify the caveats and underline how the field is ripe to overcome them. In a final chapter, I describe my part in two collaborative efforts, one to develop an image-based tracker, and the second to develop a classifier for ant behaviour. AU - Casillas Perez, Barbara E ID - 6435 KW - Social Immunity KW - Sanitary care KW - Social Insects KW - Organisational Immunity KW - Colony development KW - Multi-target tracking SN - 2663-337X TI - Collective defenses of garden ants against a fungal pathogen 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 - Insects are exposed to a variety of potential pathogens in their environment, many of which can severely impact fitness and health. Consequently, hosts have evolved resistance and tolerance strategies to suppress or cope with infections. Hosts utilizing resistance improve fitness by clearing or reducing pathogen loads, and hosts utilizing tolerance reduce harmful fitness effects per pathogen load. To understand variation in, and selective pressures on, resistance and tolerance, we asked to what degree they are shaped by host genetic background, whether plasticity in these responses depends upon dietary environment, and whether there are interactions between these two factors. Females from ten wild-type Drosophila melanogaster genotypes were kept on high- or low-protein (yeast) diets and infected with one of two opportunistic bacterial pathogens, Lactococcus lactis or Pseudomonas entomophila. We measured host resistance as the inverse of bacterial load in the early infection phase. The relationship (slope) between fly fecundity and individual-level bacteria load provided our fecundity tolerance measure. Genotype and dietary yeast determined host fecundity and strongly affected survival after infection with pathogenic P. entomophila. There was considerable genetic variation in host resistance, a commonly found phenomenon resulting from for example varying resistance costs or frequency-dependent selection. Despite this variation and the reproductive cost of higher P. entomophila loads, fecundity tolerance did not vary across genotypes. The absence of genetic variation in tolerance may suggest that at this early infection stage, fecundity tolerance is fixed or that any evolved tolerance mechanisms are not expressed under these infection conditions. AU - Kutzer, Megan AU - Kurtz, Joachim AU - Armitage, Sophie ID - 617 IS - 1 JF - Journal of Evolutionary Biology SN - 1010-061X TI - Genotype and diet affect resistance, survival, and fecundity but not fecundity tolerance VL - 31 ER - TY - JOUR AB - Sperm cells are the most morphologically diverse cells across animal taxa. Within species, sperm and ejaculate traits have been suggested to vary with the male's competitive environment, e.g., level of sperm competition, female mating status and quality, and also with male age, body mass, physiological condition, and resource availability. Most previous studies have based their conclusions on the analysis of only one or a few ejaculates per male without investigating differences among the ejaculates of the same individual. This masks potential ejaculate-specific traits. Here, we provide data on the length, quantity, and viability of sperm ejaculated by wingless males of the ant Cardiocondyla obscurior. Males of this ant species are relatively long-lived and can mate with large numbers of female sexuals throughout their lives. We analyzed all ejaculates across the individuals' lifespan and manipulated the availability of mating partners. Our study shows that both the number and size of sperm cells transferred during copulations differ among individuals and also among ejaculates of the same male. Sperm quality does not decrease with male age, but the variation in sperm number between ejaculates indicates that males need considerable time to replenish their sperm supplies. Producing many ejaculates in a short time appears to be traded-off against male longevity rather than sperm quality. AU - Metzler, Sina AU - Schrempf, Alexandra AU - Heinze, Jürgen ID - 426 JF - Journal of Insect Physiology TI - Individual- and ejaculate-specific sperm traits in ant males VL - 107 ER - TY - JOUR AB - Ants are emerging model systems to study cellular signaling because distinct castes possess different physiologic phenotypes within the same colony. Here we studied the functionality of inotocin signaling, an insect ortholog of mammalian oxytocin (OT), which was recently discovered in ants. In Lasius ants, we determined that specialization within the colony, seasonal factors, and physiologic conditions down-regulated the expression of the OT-like signaling system. Given this natural variation, we interrogated its function using RNAi knockdowns. Next-generation RNA sequencing of OT-like precursor knock-down ants highlighted its role in the regulation of genes involved in metabolism. Knock-down ants exhibited higher walking activity and increased self-grooming in the brood chamber. We propose that OT-like signaling in ants is important for regulating metabolic processes and locomotion. AU - Liutkeviciute, Zita AU - Gil Mansilla, Esther AU - Eder, Thomas AU - Casillas Perez, Barbara E AU - Giulia Di Giglio, Maria AU - Muratspahić, Edin AU - Grebien, Florian AU - Rattei, Thomas AU - Muttenthaler, Markus AU - Cremer, Sylvia AU - Gruber, Christian ID - 194 IS - 12 JF - The FASEB Journal SN - 08926638 TI - Oxytocin-like signaling in ants influences metabolic gene expression and locomotor activity VL - 32 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 - TY - JOUR AB - Social insects have evolved enormous capacities to collectively build nests and defend their colonies against both predators and pathogens. The latter is achieved by a combination of individual immune responses and sophisticated collective behavioral and organizational disease defenses, that is, social immunity. We investigated how the presence or absence of these social defense lines affects individual-level immunity in ant queens after bacterial infection. To this end, we injected queens of the ant Linepithema humile with a mix of gram+ and gram− bacteria or a control solution, reared them either with workers or alone and analyzed their gene expression patterns at 2, 4, 8, and 12 hr post-injection, using RNA-seq. This allowed us to test for the effect of bacterial infection, social context, as well as the interaction between the two over the course of infection and raising of an immune response. We found that social isolation per se affected queen gene expression for metabolism genes, but not for immune genes. When infected, queens reared with and without workers up-regulated similar numbers of innate immune genes revealing activation of Toll and Imd signaling pathways and melanization. Interestingly, however, they mostly regulated different genes along the pathways and showed a different pattern of overall gene up-regulation or down-regulation. Hence, we can conclude that the absence of workers does not compromise the onset of an individual immune response by the queens, but that the social environment impacts the route of the individual innate immune responses. AU - Viljakainen, Lumi AU - Jurvansuu, Jaana AU - Holmberg, Ida AU - Pamminger, Tobias AU - Erler, Silvio AU - Cremer, Sylvia ID - 29 IS - 22 JF - Ecology and Evolution SN - 20457758 TI - Social environment affects the transcriptomic response to bacteria in ant queens VL - 8 ER - TY - JOUR AB - Social insect colonies have evolved many collectively performed adaptations that reduce the impact of infectious disease and that are expected to maximize their fitness. This colony-level protection is termed social immunity, and it enhances the health and survival of the colony. In this review, we address how social immunity emerges from its mechanistic components to produce colony-level disease avoidance, resistance, and tolerance. To understand the evolutionary causes and consequences of social immunity, we highlight the need for studies that evaluate the effects of social immunity on colony fitness. We discuss the role that host life history and ecology have on predicted eco-evolutionary dynamics, which differ among the social insect lineages. Throughout the review, we highlight current gaps in our knowledge and promising avenues for future research, which we hope will bring us closer to an integrated understanding of socio-eco-evo-immunology. AU - Cremer, Sylvia AU - Pull, Christopher AU - Fürst, Matthias ID - 806 JF - Annual Review of Entomology SN - 1545-4487 TI - Social immunity: Emergence and evolution of colony-level disease protection VL - 63 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 - Background: The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has now been demonstrated in a wide range of invertebrate species. Despite accumulating phenotypic evidence, knowledge of its mechanistic underpinnings is currently very limited. Here we used the system of the red flour beetle, Tribolium castaneum and the insect pathogen Bacillus thuringiensis (Bt) to further our molecular understanding of the oral immune priming phenomenon. We addressed how ingestion of bacterial cues (derived from spore supernatants) of an orally pathogenic and non-pathogenic Bt strain affects gene expression upon later challenge exposure, using a whole-transcriptome sequencing approach. Results: Whereas gene expression of individuals primed with the orally non-pathogenic strain showed minor changes to controls, we found that priming with the pathogenic strain induced regulation of a large set of distinct genes, many of which are known immune candidates. Intriguingly, the immune repertoire activated upon priming and subsequent challenge qualitatively differed from the one mounted upon infection with Bt without previous priming. Moreover, a large subset of priming-specific genes showed an inverse regulation compared to their regulation upon challenge only. Conclusions: Our data demonstrate that gene expression upon infection is strongly affected by previous immune priming. We hypothesise that this shift in gene expression indicates activation of a more targeted and efficient response towards a previously encountered pathogen, in anticipation of potential secondary encounter. AU - Greenwood, Jenny AU - Milutinovic, Barbara AU - Peuß, Robert AU - Behrens, Sarah AU - Essar, Daniela AU - Rosenstiel, Philip AU - Schulenburg, Hinrich AU - Kurtz, Joachim ID - 1006 IS - 1 JF - BMC Genomics SN - 14712164 TI - Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae VL - 18 ER - TY - GEN AB - Lists of all differentially expressed genes in the different priming-challenge treatments (compared to the fully naïve control; xlsx file). Relevant columns include the following: sample_1 and sample_2 – treatment groups being compared; Normalised FPKM sample_1 and sample_2 – FPKM of samples being compared; log2(fold_change) – log2(FPKM sample 2/FPKM sample 1), i.e. negative means sample 1 upregulated compared with sample 2, positive means sample 2 upregulated compared with sample 1; cuffdiff test_statistic – test statistic of differential expression test; p_value – p-value of differential expression test; q_value (FDR correction) – adjusted P-value of differential expression test. (XLSX 598 kb) AU - Greenwood, Jenny AU - Milutinovic, Barbara AU - Peuß, Robert AU - Behrens, Sarah AU - Essar, Daniela AU - Rosenstiel, Philip AU - Schulenburg, Hinrich AU - Kurtz, Joachim ID - 9859 TI - Additional file 1: Table S1. of Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae ER - TY - GEN AU - Greenwood, Jenny AU - Milutinovic, Barbara AU - Peuß, Robert AU - Behrens, Sarah AU - Essar, Daniela AU - Rosenstiel, Philip AU - Schulenburg, Hinrich AU - Kurtz, Joachim ID - 9860 TI - Additional file 5: Table S3. of Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae 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 - Social insect societies are long-standing models for understanding social behaviour and evolution. Unlike other advanced biological societies (such as the multicellular body), the component parts of social insect societies can be easily deconstructed and manipulated. Recent methodological and theoretical innovations have exploited this trait to address an expanded range of biological questions. We illustrate the broadening range of biological insight coming from social insect biology with four examples. These new frontiers promote open-minded, interdisciplinary exploration of one of the richest and most complex of biological phenomena: sociality. AU - Kennedy, Patrick AU - Baron, Gemma AU - Qiu, Bitao AU - Freitak, Dalial AU - Helantera, Heikki AU - Hunt, Edmund AU - Manfredini, Fabio AU - O'Shea Wheller, Thomas AU - Patalano, Solenn AU - Pull, Christopher AU - Sasaki, Takao AU - Taylor, Daisy AU - Wyatt, Christopher AU - Sumner, Seirian ID - 734 IS - 11 JF - Trends in Ecology and Evolution SN - 01695347 TI - Deconstructing superorganisms and societies to address big questions in biology VL - 32 ER - TY - THES AB - Contagious diseases must transmit from infectious to susceptible hosts in order to reproduce. Whilst vectored pathogens can rely on intermediaries to find new hosts for them, many infectious pathogens require close contact or direct interaction between hosts for transmission. Hence, this means that conspecifics are often the main source of infection for most animals and so, in theory, animals should avoid conspecifics to reduce their risk of infection. Of course, in reality animals must interact with one another, as a bare minimum, to mate. However, being social provides many additional benefits and group living has become a taxonomically diverse and widespread trait. How then do social animals overcome the issue of increased disease? Over the last few decades, the social insects (ants, termites and some bees and wasps) have become a model system for studying disease in social animals. On paper, a social insect colony should be particularly susceptible to disease, given that they often contain thousands of potential hosts that are closely related and frequently interact, as well as exhibiting stable environmental conditions that encourage microbial growth. Yet, disease outbreaks appear to be rare and attempts to eradicate pest species using pathogens have failed time and again. Evolutionary biologists investigating this observation have discovered that the reduced disease susceptibility in social insects is, in part, due to collectively performed disease defences of the workers. These defences act like a “social immune system” for the colony, resulting in a per capita decrease in disease, termed social immunity. Our understanding of social immunity, and its importance in relation to the immunological defences of each insect, continues to grow, but there remain many open questions. In this thesis I have studied disease defence in garden ants. In the first data chapter, I use the invasive garden ant, Lasius neglectus, to investigate how colonies mitigate lethal infections and prevent them from spreading systemically. I find that ants have evolved ‘destructive disinfection’ – a behaviour that uses endogenously produced acidic poison to kill diseased brood and to prevent the pathogen from replicating. In the second experimental chapter, I continue to study the use of poison in invasive garden ant colonies, finding that it is sprayed prophylactically within the nest. However, this spraying has negative effects on developing pupae when they have had their cocoons artificially removed. Hence, I suggest that acidic nest sanitation may be maintaining larval cocoon spinning in this species. In the next experimental chapter, I investigated how colony founding black garden ant queens (Lasius niger) prevent disease when a co-foundress dies. I show that ant queens prophylactically perform undertaking behaviours, similar to those performed by the workers in mature nests. When a co-foundress was infected, these undertaking behaviours improved the survival of the healthy queen. In the final data chapter, I explored how immunocompetence (measured as antifungal activity) changes as incipient black garden ant colonies grow and mature, from the solitary queen phase to colonies with several hundred workers. Queen and worker antifungal activity varied throughout this time period, but despite social immunity, did not decrease as colonies matured. In addition to the above data chapters, this thesis includes two co-authored reviews. In the first, we examine the state of the art in the field of social immunity and how it might develop in the future. In the second, we identify several challenges and open questions in the study of disease defence in animals. We highlight how social insects offer a unique model to tackle some of these problems, as disease defence can be studied from the cell to the society. AU - Pull, Christopher ID - 819 SN - 2663-337X TI - Disease defence in garden ants ER - TY - JOUR AB - Background: Social insects form densely crowded societies in environments with high pathogen loads, but have evolved collective defences that mitigate the impact of disease. However, colony-founding queens lack this protection and suffer high rates of mortality. The impact of pathogens may be exacerbated in species where queens found colonies together, as healthy individuals may contract pathogens from infectious co-founders. Therefore, we tested whether ant queens avoid founding colonies with pathogen-exposed conspecifics and how they might limit disease transmission from infectious individuals. Results: Using Lasius Niger queens and a naturally infecting fungal pathogen Metarhizium brunneum, we observed that queens were equally likely to found colonies with another pathogen-exposed or sham-treated queen. However, when one queen died, the surviving individual performed biting, burial and removal of the corpse. These undertaking behaviours were performed prophylactically, i.e. targeted equally towards non-infected and infected corpses, as well as carried out before infected corpses became infectious. Biting and burial reduced the risk of the queens contracting and dying from disease from an infectious corpse of a dead co-foundress. Conclusions: We show that co-founding ant queens express undertaking behaviours that, in mature colonies, are performed exclusively by workers. Such infection avoidance behaviours act before the queens can contract the disease and will therefore improve the overall chance of colony founding success in ant queens. AU - Pull, Christopher AU - Cremer, Sylvia ID - 732 IS - 1 JF - BMC Evolutionary Biology SN - 14712148 TI - Co-founding ant queens prevent disease by performing prophylactic undertaking behaviour VL - 17 ER - TY - JOUR AB - The social insects bees, wasps, ants, and termites are species-rich, occur in many habitats, and often constitute a large part of the biomass. Many are also invasive, including species of termites, the red imported fire ant, and the Argentine ant. While invasive social insects have been a problem in Southern Europe for some time, Central Europa was free of invasive ant species until recently because most ants are adapted to warmer climates. Only in the 1990s, did Lasius neglectus, a close relative of the common black garden ant, arrive in Germany. First described in 1990 based on individuals collected in Budapest, the species has since been detected for example in France, Germany, Spain, England, and Kyrgyzstan. The species is spread with soil during construction work or plantings, and L. neglectus therefore is often found in parks and botanical gardens. Another invasive ant now spreading in southern Germany is Formica fuscocinerea, which occurs along rivers, including in the sandy floodplains of the river Isar. As is typical of pioneer species, F. fuscocinerea quickly becomes extremely abundant and therefore causes problems for example on playgrounds in Munich. All invasive ant species are characterized by cooperation across nests, leading to strongly interconnected, very large super-colonies. The resulting dominance results in the extinction of native ant species as well as other arthropod species and thus in the reduction of biodiversity. AU - Cremer, Sylvia ID - 459 JF - Rundgespräche Forum Ökologie SN - 2366-2875 TI - Invasive Ameisen in Europa: Wie sie sich ausbreiten und die heimische Fauna verändern VL - 46 ER - TY - JOUR AB - Immune specificity is the degree to which a host’s immune system discriminates among various pathogens or antigenic variants. Vertebrate immune memory is highly specific due to antibody responses. On the other hand, some invertebrates show immune priming, i.e. improved survival after secondary exposure to a previously encountered pathogen. Until now, specificity of priming has only been demonstrated via the septic infection route or when live pathogens were used for priming. Therefore, we tested for specificity in the oral priming route in the red flour beetle, Tribolium castaneum. For priming, we used pathogen-free supernatants derived from three different strains of the entomopathogen, Bacillus thuringiensis, which express different Cry toxin variants known for their toxicity against this beetle. Subsequent exposure to the infective spores showed that oral priming was specific for two naturally occurring strains, while a third engineered strain did not induce any priming effect. Our data demonstrate that oral immune priming with a non-infectious bacterial agent can be specific, but the priming effect is not universal across all bacterial strains. AU - Futo, Momir AU - Sell, Marie AU - Kutzer, Megan AU - Kurtz, Joachim ID - 558 IS - 12 JF - Biology Letters SN - 1744-9561 TI - Specificity of oral immune priming in the red flour beetle Tribolium castaneum VL - 13 ER - TY - JOUR AB - Across multicellular organisms, the costs of reproduction and self-maintenance result in a life history trade-off between fecundity and longevity. Queens of perennial social Hymenoptera are both highly fertile and long-lived, and thus, this fundamental trade-off is lacking. Whether social insect males similarly evade the fecundity/longevity trade-off remains largely unstudied. Wingless males of the ant genus Cardiocondyla stay in their natal colonies throughout their relatively long lives and mate with multiple female sexuals. Here, we show that Cardiocondyla obscurior males that were allowed to mate with large numbers of female sexuals had a shortened life span compared to males that mated at a low frequency or virgin males. Although frequent mating negatively affects longevity, males clearly benefit from a “live fast, die young strategy” by inseminating as many female sexuals as possible at a cost to their own survival. AU - Metzler, Sina AU - Heinze, Jürgen AU - Schrempf, Alexandra ID - 1184 IS - 24 JF - Ecology and Evolution TI - Mating and longevity in ant males VL - 6 ER - TY - JOUR AU - Milutinovic, Barbara AU - Peuß, Robert AU - Ferro, Kevin AU - Kurtz, Joachim ID - 1202 IS - 4 JF - Zoology TI - Immune priming in arthropods: an update focusing on the red flour beetle VL - 119 ER - TY - JOUR AB - Down syndrome cell adhesion molecule 1 (Dscam1) has widereaching and vital neuronal functions although the role it plays in insect and crustacean immunity is less well understood. In this study, we combine different approaches to understand the roles that Dscam1 plays in fitness-related contexts in two model insect species. Contrary to our expectations, we found no short-term modulation of Dscam1 gene expression after haemocoelic or oral bacterial exposure in Tribolium castaneum, or after haemocoelic bacterial exposure in Drosophila melanogaster. Furthermore, RNAi-mediated Dscam1 knockdown and subsequent bacterial exposure did not reduce T. castaneum survival. However, Dscam1 knockdown in larvae resulted in adult locomotion defects, as well as dramatically reduced fecundity in males and females. We suggest that Dscam1 does not always play a straightforward role in immunity, but strongly influences behaviour and fecundity. This study takes a step towards understanding more about the role of this intriguing gene from different phenotypic perspectives. AU - Peuß, Robert AU - Wensing, Kristina AU - Woestmann, Luisa AU - Eggert, Hendrik AU - Milutinovic, Barbara AU - Sroka, Marlene AU - Scharsack, Jörn AU - Kurtz, Joachim AU - Armitage, Sophie ID - 1255 IS - 4 JF - Royal Society Open Science TI - Down syndrome cell adhesion molecule 1: Testing for a role in insect immunity, behaviour and reproduction VL - 3 ER - TY - JOUR AU - Milutinovic, Barbara AU - Kurtz, Joachim ID - 1268 IS - 4 JF - Seminars in Immunology TI - Immune memory in invertebrates VL - 28 ER - TY - JOUR AB - The rare socially parasitic butterfly Maculinea alcon occurs in two forms, which are characteristic of hygric or xeric habitats and which exploit different host plants and host ants. The status of these two forms has been the subject of considerable controversy. Populations of the two forms are usually spatially distinct, but at Răscruci in Romania both forms occur on the same site (syntopically). We examined the genetic differentiation between the two forms using eight microsatellite markers, and compared with a nearby hygric site, Şardu. Our results showed that while the two forms are strongly differentiated at Răscruci, it is the xeric form there that is most similar to the hygric form at Şardu, and Bayesian clustering algorithms suggest that these two populations have exchanged genes relatively recently. We found strong evidence for population substructuring, caused by high within host ant nest relatedness, indicating very limited dispersal of most ovipositing females, but not association with particular host ant species. Our results are consistent with the results of larger scale phylogeographic studies that suggest that the two forms represent local ecotypes specialising on different host plants, each with a distinct flowering phenology, providing a temporal rather than spatial barrier to gene flow. AU - Tartally, András AU - Kelager, Andreas AU - Fürst, Matthias AU - Nash, David ID - 1431 IS - 3 JF - PeerJ TI - Host plant use drives genetic differentiation in syntopic populations of Maculinea alcon VL - 2016 ER - TY - GEN AB - Summary: Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses. Within a structured large-scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co-occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species-specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations. Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline. AU - Mcmahon, Dino AU - Fürst, Matthias AU - Caspar, Jesicca AU - Theodorou, Panagiotis AU - Brown, Mark AU - Paxton, Robert ID - 9720 TI - Data from: A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees ER - TY - JOUR AB - Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline. AU - Mcmahon, Dino AU - Natsopoulou, Myrsini AU - Doublet, Vincent AU - Fürst, Matthias AU - Weging, Silvio AU - Brown, Mark AU - Gogol Döring, Andreas AU - Paxton, Robert ID - 1262 IS - 1833 JF - Proceedings of the Royal Society of London Series B Biological Sciences TI - Elevated virulence of an emerging viral genotype as a driver of honeybee loss VL - 283 ER - TY - GEN AB - Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline. AU - Mcmahon, Dino AU - Natsopoulou, Myrsini AU - Doublet, Vincent AU - Fürst, Matthias AU - Weging, Silvio AU - Brown, Mark AU - Gogol Döring, Andreas AU - Paxton, Robert ID - 9704 TI - Data from: Elevated virulence of an emerging viral genotype as a driver of honeybee loss ER - TY - JOUR AB - Reciprocal coevolution between host and pathogen is widely seen as a major driver of evolution and biological innovation. Yet, to date, the underlying genetic mechanisms and associated trait functions that are unique to rapid coevolutionary change are generally unknown. We here combined experimental evolution of the bacterial biocontrol agent Bacillus thuringiensis and its nematode host Caenorhabditis elegans with large-scale phenotyping, whole genome analysis, and functional genetics to demonstrate the selective benefit of pathogen virulence and the underlying toxin genes during the adaptation process. We show that: (i) high virulence was specifically favoured during pathogen–host coevolution rather than pathogen one-sided adaptation to a nonchanging host or to an environment without host; (ii) the pathogen genotype BT-679 with known nematocidal toxin genes and high virulence specifically swept to fixation in all of the independent replicate populations under coevolution but only some under one-sided adaptation; (iii) high virulence in the BT-679-dominated populations correlated with elevated copy numbers of the plasmid containing the nematocidal toxin genes; (iv) loss of virulence in a toxin-plasmid lacking BT-679 isolate was reconstituted by genetic reintroduction or external addition of the toxins.We conclude that sustained coevolution is distinct from unidirectional selection in shaping the pathogen's genome and life history characteristics. To our knowledge, this study is the first to characterize the pathogen genes involved in coevolutionary adaptation in an animal host–pathogen interaction system. AU - El Masri, Leila AU - Branca, Antoine AU - Sheppard, Anna AU - Papkou, Andrei AU - Laehnemann, David AU - Guenther, Patrick AU - Prahl, Swantje AU - Saebelfeld, Manja AU - Hollensteiner, Jacqueline AU - Liesegang, Heiko AU - Brzuszkiewicz, Elzbieta AU - Daniel, Rolf AU - Michiels, Nico AU - Schulte, Rebecca AU - Kurtz, Joachim AU - Rosenstiel, Philip AU - Telschow, Arndt AU - Bornberg Bauer, Erich AU - Schulenburg, Hinrich ID - 1551 IS - 6 JF - PLoS Biology TI - Host–pathogen coevolution: The selective advantage of Bacillus thuringiensis virulence and its cry toxin genes VL - 13 ER - TY - JOUR AB - Reproduction within a host and transmission to the next host are crucial for the virulence and fitness of pathogens. Nevertheless, basic knowledge about such parameters is often missing from the literature, even for well-studied bacteria, such as Bacillus thuringiensis, an endospore-forming insect pathogen, which infects its hosts via the oral route. To characterize bacterial replication success, we made use of an experimental oral infection system for the red flour beetle Tribolium castaneum and developed a flow cytometric assay for the quantification of both spore ingestion by the individual beetle larvae and the resulting spore load after bacterial replication and resporulation within cadavers. On average, spore numbers increased 460-fold, showing that Bacillus thuringiensis grows and replicates successfully in insect cadavers. By inoculating cadaver-derived spores and spores from bacterial stock cultures into nutrient medium, we next investigated outgrowth characteristics of vegetative cells and found that cadaver- derived bacteria showed reduced growth compared to bacteria from the stock cultures. Interestingly, this reduced growth was a consequence of inhibited spore germination, probably originating from the host and resulting in reduced host mortality in subsequent infections by cadaver-derived spores. Nevertheless, we further showed that Bacillus thuringiensis transmission was possible via larval cannibalism when no other food was offered. These results contribute to our understanding of the ecology of Bacillus thuringiensis as an insect pathogen. AU - Milutinovic, Barbara AU - Höfling, Christina AU - Futo, Momir AU - Scharsack, Jörn AU - Kurtz, Joachim ID - 1548 IS - 23 JF - Applied and Environmental Microbiology TI - Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination VL - 81 ER - TY - JOUR AB - This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research. AU - Kappeler, Peter AU - Cremer, Sylvia AU - Nunn, Charles ID - 1831 IS - 1669 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences TI - Sociality and health: Impacts of sociality on disease susceptibility and transmission in animal and human societies VL - 370 ER - TY - JOUR AB - Entomopathogenic fungi are potent biocontrol agents that are widely used against insect pests, many of which are social insects. Nevertheless, theoretical investigations of their particular life history are scarce. We develop a model that takes into account the main distinguishing features between traditionally studied diseases and obligate killing pathogens, like the (biocontrol-relevant) insect-pathogenic fungi Metarhizium and Beauveria. First, obligate killing entomopathogenic fungi produce new infectious particles (conidiospores) only after host death and not yet on the living host. Second, the killing rates of entomopathogenic fungi depend strongly on the initial exposure dosage, thus we explicitly consider the pathogen load of individual hosts. Further, we make the model applicable not only to solitary host species, but also to group living species by incorporating social interactions between hosts, like the collective disease defences of insect societies. Our results identify the optimal killing rate for the pathogen that minimises its invasion threshold. Furthermore, we find that the rate of contact between hosts has an ambivalent effect: dense interaction networks between individuals are considered to facilitate disease outbreaks because of increased pathogen transmission. In social insects, this is compensated by their collective disease defences, i.e., social immunity. For the type of pathogens considered here, we show that even without social immunity, high contact rates between live individuals dilute the pathogen in the host colony and hence can reduce individual pathogen loads below disease-causing levels. AU - Novak, Sebastian AU - Cremer, Sylvia ID - 1850 IS - 5 JF - Journal of Theoretical Biology TI - Fungal disease dynamics in insect societies: Optimal killing rates and the ambivalent effect of high social interaction rates VL - 372 ER - TY - JOUR AB - Summary: Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses. Within a structured large-scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co-occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species-specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations. Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline. AU - Mcmahon, Dino AU - Fürst, Matthias AU - Caspar, Jesicca AU - Theodorou, Panagiotis AU - Brown, Mark AU - Paxton, Robert ID - 1855 IS - 3 JF - Journal of Animal Ecology TI - A sting in the spit: Widespread cross-infection of multiple RNA viruses across wild and managed bees VL - 84 ER - TY - JOUR AB - 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. AU - Theis, Fabian AU - Ugelvig, Line V AU - Marr, Carsten AU - Cremer, Sylvia ID - 1830 IS - 1669 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences SN - 0962-8436 TI - Opposing effects of allogrooming on disease transmission in ant societies VL - 370 ER - TY - GEN AB - 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. AU - Theis, Fabian AU - Ugelvig, Line V AU - Marr, Carsten AU - Cremer, Sylvia ID - 9721 TI - Data from: Opposing effects of allogrooming on disease transmission in ant societies 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 - GEN AB - Repeated pathogen exposure is a common threat in colonies of social insects, posing selection pressures on colony members to respond with improved disease-defense performance. We here tested whether experience gained by repeated tending of low-level fungus-exposed (Metarhizium robertsii) larvae may alter the performance of sanitary brood care in the clonal ant, Platythyrea punctata. We trained ants individually over nine consecutive trials to either sham-treated or fungus-exposed larvae. We then compared the larval grooming behavior of naive and trained ants and measured how effectively they removed infectious fungal conidiospores from the fungus-exposed larvae. We found that the ants changed the duration of larval grooming in response to both, larval treatment and their level of experience: (1) sham-treated larvae received longer grooming than the fungus-exposed larvae and (2) trained ants performed less self-grooming but longer larval grooming than naive ants, which was true for both, ants trained to fungus-exposed and also to sham-treated larvae. Ants that groomed the fungus-exposed larvae for longer periods removed a higher number of fungal conidiospores from the surface of the fungus-exposed larvae. As experienced ants performed longer larval grooming, they were more effective in fungal removal, thus making them better caretakers under pathogen attack of the colony. By studying this clonal ant, we can thus conclude that even in the absence of genetic variation between colony members, differences in experience levels of brood care may affect performance of sanitary brood care in social insects. AU - Westhus, Claudia AU - Ugelvig, Line V AU - Tourdot, Edouard AU - Heinze, Jürgen AU - Doums, Claudie AU - Cremer, Sylvia ID - 9742 TI - Data from: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant ER - TY - THES AB - The co-evolution of hosts and pathogens is characterized by continuous adaptations of both parties. Pathogens of social insects need to adapt towards disease defences at two levels: 1) individual immunity of each colony member consisting of behavioural defence strategies as well as humoral and cellular immune responses and 2) social immunity that is collectively performed by all group members comprising behavioural, physiological and organisational defence strategies. To disentangle the selection pressure on pathogens by the collective versus individual level of disease defence in social insects, we performed an evolution experiment using the Argentine Ant, Linepithema humile, as a host and a mixture of the general insect pathogenic fungus Metarhizium spp. (6 strains) as a pathogen. We allowed pathogen evolution over 10 serial host passages to two different evolution host treatments: (1) only individual host immunity in a single host treatment, and (2) simultaneously acting individual and social immunity in a social host treatment, in which an exposed ant was accompanied by two untreated nestmates. Before starting the pathogen evolution experiment, the 6 Metarhizium spp. strains were characterised concerning conidiospore size killing rates in singly and socially reared ants, their competitiveness under coinfecting conditions and their influence on ant behaviour. We analysed how the ancestral atrain mixture changed in conidiospere size, killing rate and strain composition dependent on host treatment (single or social hosts) during 10 passages and found that killing rate and conidiospere size of the pathogen increased under both evolution regimes, but different depending on host treatment. Testing the evolved strain mixtures that evolved under either the single or social host treatment under both single and social current rearing conditions in a full factorial design experiment revealed that the additional collective defences in insect societies add new selection pressure for their coevolving pathogens that compromise their ability to adapt to its host at the group level. To our knowledge, this is the first study directly measuring the influence of social immunity on pathogen evolution. AU - Stock, Miriam ID - 1404 TI - Evolution of a fungal pathogen towards individual versus social immunity in ants 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 - JOUR AB - Immune systems are able to protect the body against secondary infection with the same parasite. In insect colonies, this protection is not restricted to the level of the individual organism, but also occurs at the societal level. Here, we review recent evidence for and insights into the mechanisms underlying individual and social immunisation in insects. We disentangle general immune-protective effects from specific immune memory (priming), and examine immunisation in the context of the lifetime of an individual and that of a colony, and of transgenerational immunisation that benefits offspring. When appropriate, we discuss parallels with disease defence strategies in human societies. We propose that recurrent parasitic threats have shaped the evolution of both the individual immune systems and colony-level social immunity in insects. AU - El Masri, Leila AU - Cremer, Sylvia ID - 1998 IS - 10 JF - Trends in Immunology TI - Individual and social immunisation in insects VL - 35 ER - TY - JOUR AB - Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline, one cause of which may be pathogen spillover from managed pollinators like honeybees or commercial colonies of bumblebees. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators. AU - Fürst, Matthias AU - Mcmahon, Dino AU - Osborne, Juliet AU - Paxton, Robert AU - Brown, Mark ID - 2235 IS - 7488 JF - Nature SN - 00280836 TI - Disease associations between honeybees and bumblebees as a threat to wild pollinators VL - 506 ER - TY - JOUR AB - Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen - Nosema ceranae (Microsporidia) - on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed. AU - Wolf, Stephan AU - Mcmahon, Dino AU - Lim, Ka AU - Pull, Christopher AU - Clark, Suzanne AU - Paxton, Robert AU - Osborne, Juliet ID - 2086 IS - 8 JF - PLoS One TI - So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees VL - 9 ER - TY - GEN AB - Detailed description of the experimental prodedures, data analyses and additional statistical analyses of the results. AU - Wolf, Stephan AU - Mcmahon, Dino AU - Lim, Ka AU - Pull, Christopher AU - Clark, Suzanne AU - Paxton, Robert AU - Osborne, Juliet ID - 9888 TI - Supporting information ER - TY - JOUR AB - Repeated pathogen exposure is a common threat in colonies of social insects, posing selection pressures on colony members to respond with improved disease-defense performance. We here tested whether experience gained by repeated tending of low-level fungus-exposed (Metarhizium robertsii) larvae may alter the performance of sanitary brood care in the clonal ant, Platythyrea punctata. We trained ants individually over nine consecutive trials to either sham-treated or fungus-exposed larvae. We then compared the larval grooming behavior of naive and trained ants and measured how effectively they removed infectious fungal conidiospores from the fungus-exposed larvae. We found that the ants changed the duration of larval grooming in response to both, larval treatment and their level of experience: (1) sham-treated larvae received longer grooming than the fungus-exposed larvae and (2) trained ants performed less self-grooming but longer larval grooming than naive ants, which was true for both, ants trained to fungus-exposed and also to sham-treated larvae. Ants that groomed the fungus-exposed larvae for longer periods removed a higher number of fungal conidiospores from the surface of the fungus-exposed larvae. As experienced ants performed longer larval grooming, they were more effective in fungal removal, thus making them better caretakers under pathogen attack of the colony. By studying this clonal ant, we can thus conclude that even in the absence of genetic variation between colony members, differences in experience levels of brood care may affect performance of sanitary brood care in social insects. AU - Westhus, Claudia AU - Ugelvig, Line V AU - Tourdot, Edouard AU - Heinze, Jürgen AU - Doums, Claudie AU - Cremer, Sylvia ID - 2161 IS - 10 JF - Behavioral Ecology and Sociobiology SN - 0340-5443 TI - Increased grooming after repeated brood care provides sanitary benefits in a clonal ant VL - 68 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 - TY - GEN AB - 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. AU - Tragust, Simon AU - Ugelvig, Line V AU - Chapuisat, Michel AU - Heinze, Jürgen AU - Cremer, Sylvia ID - 9753 TI - Data from: Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies ER - TY - THES AB - In this thesis I studied various individual and social immune defences employed by the invasive garden ant Lasius neglectus mostly against entomopathogenic fungi. The first two chapters of this thesis address the phenomenon of 'social immunisation'. Social immunisation, that is the immunological protection of group members due to social contact to a pathogen-exposed nestmate, has been described in various social insect species against different types of pathogens. However, in the case of entomopathogenic fungi it has, so far, only been demonstrated that social immunisation exists at all. Its underlying mechanisms r any other properties were, however, unknown. In the first chapter of this thesis I identified the mechanistic basis of social immunisation in L. neglectus against the entomopathogenous fungus Metarhizium. I could show that nestmates of a pathogen-exposed individual contract low-level infections due to social interactions. These low-level infections are, however, non-lethal and cause an active stimulation of the immune system, which protects the nestmates upon subsequent pathogen encounters. In the second chapter of this thesis I investigated the specificity and colony level effects of social immunisation. I demonstrated that the protection conferred by social immunisation is highly specific, protecting ants only against the same pathogen strain. In addition, depending on the respective context, social immunisation may even cause fitness costs. I further showed that social immunisation crucially affects sanitary behaviour and disease dynamics within ant groups. In the third chapter of this thesis I studied the effects of the ectosymbiotic fungus Laboulbenia formicarum on its host L. neglectus. Although Laboulbeniales are the largest order of insect-parasitic fungi, research concerning host fitness consequence is sparse. I showed that highly Laboulbenia-infected ants sustain fitness costs under resource limitation, however, gain fitness benefits when exposed to an entomopathogenus fungus. These effects are probably cause by a prophylactic upregulation of behavioural as well as physiological immune defences in highly infected ants. AU - Konrad, Matthias ID - 1395 SN - 2663-337X TI - Immune defences in ants: Effects of social immunisation and a fungal ectosymbiont in the ant Lasius neglectus ER - TY - JOUR AU - Cremer, Sylvia ID - 1887 JF - Zoologie TI - Gemeinsame Krankheitsabwehr in Ameisengesellschaften ER - TY - CHAP AB - Im Rahmen meiner Arbeit mit der kollektiven Krankheitsabwehr in Ameisengesellschaften interessiert mich vor allem, wie sich die Kolonien als Ganzes gegen Krankheiten wehren können. Warum ist dieses Thema der Krankheitsdynamik in Gruppen so wichtig? Ein Vergleich von solitär lebenden Individuen mit Individuen, die in sozialen Gruppen zusammenleben, zeigt die Kosten und die Vorteile des Gruppenlebens: Einerseits haben Individuen in sozialen Gruppen aufgrund der hohen Dichte, in der die Tiere zusammenleben, den hohen Interaktionsraten, die sie miteinander haben, und der engen Verwandtschaft, die sie verbindet, ein höheres Ansteckungsrisiko. Andererseits kann die individuelle Krankheitsabwehr durch die kollektive Abwehr in den Gruppen ergänzt werden. AU - Cremer, Sylvia ID - 1888 SN - 2366-2875 T2 - Soziale Insekten in einer sich wandelnden Welt TI - Soziale Immunität: Wie sich der Staat gegen Pathogene wehrt Bayerische Akademie der Wissenschaften VL - 43 ER - TY - JOUR AB - Selection for disease control is believed to have contributed to shape the organisation of insect societies — leading to interaction patterns that mitigate disease transmission risk within colonies, conferring them ‘organisational immunity’. Recent studies combining epidemiological models with social network analysis have identified general properties of interaction networks that may hinder propagation of infection within groups. These can be prophylactic and/or induced upon pathogen exposure. Here we review empirical evidence for these two types of organisational immunity in social insects and describe the individual-level behaviours that underlie it. We highlight areas requiring further investigation, and emphasise the need for tighter links between theory and empirical research and between individual-level and collective-level analyses. AU - Stroeymeyt, Nathalie AU - Casillas Perez, Barbara E AU - Cremer, Sylvia ID - 1999 IS - 1 JF - Current Opinion in Insect Science TI - Organisational immunity in social insects VL - 5 ER - TY - JOUR AB - Pathogens exert a strong selection pressure on organisms to evolve effective immune defences. In addition to individual immunity, social organisms can act cooperatively to produce collective defences. In many ant species, queens have the option to found a colony alone or in groups with other, often unrelated, conspecifics. These associations are transient, usually lasting only as long as each queen benefits from the presence of others. In fact, once the first workers emerge, queens fight to the death for dominance. One potential advantage of co-founding may be that queens benefit from collective disease defences, such as mutual grooming, that act against common soil pathogens. We test this hypothesis by exposing single and co-founding queens to a fungal parasite, in order to assess whether queens in co-founding associations have improved survival. Surprisingly, co-foundresses exposed to the entomopathogenic fungus Metarhizium did not engage in cooperative disease defences, and consequently, we find no direct benefit of multiple queens on survival. However, an indirect benefit was observed, with parasite-exposed queens producing more brood when they co-founded, than when they were alone. We suggest this is due to a trade-off between reproduction and immunity. Additionally, we report an extraordinary ability of the queens to tolerate an infection for long periods after parasite exposure. Our study suggests that there are no social immunity benefits for co-founding ant queens, but that in parasite-rich environments, the presence of additional queens may nevertheless improve the chances of colony founding success. AU - Pull, Christopher AU - Hughes, William AU - Brown, Markus ID - 2283 IS - 12 JF - Naturwissenschaften TI - Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger VL - 100 ER - TY - JOUR AB - 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. AU - Tragust, Simon AU - Ugelvig, Line V AU - Chapuisat, Michel AU - Heinze, Jürgen AU - Cremer, Sylvia ID - 2284 IS - 1 JF - BMC Evolutionary Biology TI - Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies VL - 13 ER - TY - JOUR AB - 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. AU - Tragust, Simon AU - Mitteregger, Barbara AU - Barone, Vanessa AU - Konrad, Matthias AU - Ugelvig, Line V AU - Cremer, Sylvia ID - 2926 IS - 1 JF - Current Biology TI - Ants disinfect fungus-exposed brood by oral uptake and spread of their poison VL - 23 ER - TY - JOUR AB - Social insects have a very high potential to become invasive pest species. Here, we explore how their social lifestyle and their interaction with parasites may contribute to this invasive success. Similar to solitary species, parasite release followed by the evolution of increased competitive ability can promote establishment of introduced social insect hosts in their introduced range. Genetic bottlenecks during introduction of low numbers of founder individuals decrease the genetic diversity at three levels: the population, the colony and the individual, with the colony level being specific to social insects. Reduced genetic diversity can affect both the individual immune system and the collective colony-level disease defences (social immunity). Still, the dual immune system is likely to make social insects more robust to parasite attack. Changes in social structure from small, family-based, territorially aggressive societies in native populations towards huge networks of cooperating nests (unicoloniality) occur in some invasive social insects, for example, most invasive ants and some termites. Unicoloniality is likely to affect disease dynamics in multiple ways. The free exchange of individuals within the population leads to an increased genetic heterogeneity among individuals of a single nest, thereby decreasing disease transmission. However, the multitude of reproductively active queens per colony buffers the effect of individual diseased queens and their offspring, which may result in a higher level of vertical disease transmission in unicolonial societies. Lastly, unicoloniality provides a competitive advantage over native species, allowing them to quickly become the dominant species in the habitat, which in turn selects for parasite adaptation to this common host genotype and thus eventually a high parasite pressure. Overall, invasions by insect societies are characterized by general features applying to all introduced species, as well as idiosyncrasies that emerge from their social lifestyle. It is important to study these effects in concert to be able to develop efficient management and biocontrol strategies. © 2012 British Ecological Society. AU - Ugelvig, Line V AU - Cremer, Sylvia ID - 2938 IS - 6 JF - Functional Ecology TI - Effects of social immunity and unicoloniality on host parasite interactions in invasive insect societies VL - 26 ER - TY - JOUR AB - Background: The outcome of male-male competition can be predicted from the relative fighting qualities of the opponents, which often depend on their age. In insects, freshly emerged and still sexually inactive males are morphologically indistinct from older, sexually active males. These young inactive males may thus be easy targets for older males if they cannot conceal themselves from their attacks. The ant Cardiocondyla obscurior is characterised by lethal fighting between wingless (" ergatoid" ) males. Here, we analyse for how long young males are defenceless after eclosion, and how early adult males can detect the presence of rival males.Results: We found that old ergatoid males consistently won fights against ergatoid males younger than two days. Old males did not differentiate between different types of unpigmented pupae several days before emergence, but had more frequent contact to ready-to-eclose pupae of female sexuals and winged males than of workers and ergatoid males. In rare cases, old ergatoid males displayed alleviated biting of pigmented ergatoid male pupae shortly before adult eclosion, as well as copulation attempts to dark pupae of female sexuals and winged males. Ergatoid male behaviour may be promoted by a closer similarity of the chemical profile of ready-to-eclose pupae to the profile of adults than that of young pupae several days prior to emergence.Conclusion: Young ergatoid males of C. obscurior would benefit greatly by hiding their identity from older, resident males, as they are highly vulnerable during the first two days of their adult lives. In contrast to the winged males of the same species, which are able to prevent ergatoid male attacks by chemical female mimicry, young ergatoids do not seem to be able to produce a protective chemical profile. Conflicts in male-male competition between ergatoid males of different age thus seem to be resolved in favour of the older males. This might represent selection at the colony level rather than the individual level. © 2012 Cremer et al.; licensee BioMed Central Ltd. AU - Cremer, Sylvia AU - Suefuji, Masaki AU - Schrempf, Alexandra AU - Heinze, Jürgen ID - 2966 JF - BMC Ecology TI - The dynamics of male-male competition in Cardiocondyla obscurior ants VL - 12 ER - TY - JOUR AB - Reproductive division of labour is a characteristic trait of social insects. The dominant reproductive individual, often the queen, uses chemical communication and/or behaviour to maintain her social status. Queens of many social insects communicate their fertility status via cuticle-bound substances. As these substances usually possess a low volatility, their range in queen–worker communication is potentially limited. Here, we investigate the range and impact of behavioural and chemical queen signals on workers of the ant Temnothorax longispinosus. We compared the behaviour and ovary development of workers subjected to three different treatments: workers with direct chemical and physical contact to the queen, those solely under the influence of volatile queen substances and those entirely separated from the queen. In addition to short-ranged queen signals preventing ovary development in workers, we discovered a novel secondary pathway influencing worker behaviour. Workers with no physical contact to the queen, but exposed to volatile substances, started to develop their ovaries, but did not change their behaviour compared to workers in direct contact to the queen. In contrast, workers in queen-separated groups showed both increased ovary development and aggressive dominance interactions. We conclude that T. longispinosus queens influence worker ovary development and behaviour via two independent signals, both ensuring social harmony within the colony. AU - Konrad, Matthias AU - Pamminger, Tobias AU - Foitzik, Susanne ID - 3132 IS - 8 JF - Naturwissenschaften TI - Two pathways ensuring social harmony VL - 99 ER - TY - JOUR AB - Some inflammatory stimuli trigger activation of the NLRP3 inflammasome by inducing efflux of cellular potassium. Loss of cellular potassium is known to potently suppress protein synthesis, leading us to test whether the inhibition of protein synthesis itself serves as an activating signal for the NLRP3 inflammasome. Murine bone marrow-derived macrophages, either primed by LPS or unprimed, were exposed to a panel of inhibitors of ribosomal function: ricin, cycloheximide, puromycin, pactamycin, and anisomycin. Macrophages were also exposed to nigericin, ATP, monosodium urate (MSU), and poly I:C. Synthesis of pro-IL-ß and release of IL-1ß from cells in response to these agents was detected by immunoblotting and ELISA. Release of intracellular potassium was measured by mass spectrometry. Inhibition of translation by each of the tested translation inhibitors led to processing of IL-1ß, which was released from cells. Processing and release of IL-1ß was reduced or absent from cells deficient in NLRP3, ASC, or caspase-1, demonstrating the role of the NLRP3 inflammasome. Despite the inability of these inhibitors to trigger efflux of intracellular potassium, the addition of high extracellular potassium suppressed activation of the NLRP3 inflammasome. MSU and double-stranded RNA, which are known to activate the NLRP3 inflammasome, also substantially inhibited protein translation, supporting a close association between inhibition of translation and inflammasome activation. These data demonstrate that translational inhibition itself constitutes a heretofore-unrecognized mechanism underlying IL-1ß dependent inflammatory signaling and that other physical, chemical, or pathogen-associated agents that impair translation may lead to IL-1ß-dependent inflammation through activation of the NLRP3 inflammasome. For agents that inhibit translation through decreased cellular potassium, the application of high extracellular potassium restores protein translation and suppresses activation of the NLRP inflammasome. For agents that inhibit translation through mechanisms that do not involve loss of potassium, high extracellular potassium suppresses IL-1ß processing through a mechanism that remains undefined. AU - Vyleta, Meghan AU - Wong, John AU - Magun, Bruce ID - 3161 IS - 5 JF - PLoS One TI - Suppression of ribosomal function triggers innate immune signaling through activation of the NLRP3 inflammasome VL - 7 ER - TY - JOUR AB - Dispersal is crucial for gene flow and often determines the long-term stability of meta-populations, particularly in rare species with specialized life cycles. Such species are often foci of conservation efforts because they suffer disproportionally from degradation and fragmentation of their habitat. However, detailed knowledge of effective gene flow through dispersal is often missing, so that conservation strategies have to be based on mark-recapture observations that are suspected to be poor predictors of long-distance dispersal. These constraints have been especially severe in the study of butterfly populations, where microsatellite markers have been difficult to develop. We used eight microsatellite markers to analyse genetic population structure of the Large Blue butterfly Maculinea arion in Sweden. During recent decades, this species has become an icon of insect conservation after massive decline throughout Europe and extinction in Britain followed by reintroduction of a seed population from the Swedish island of Öland. We find that populations are highly structured genetically, but that gene flow occurs over distances 15 times longer than the maximum distance recorded from mark-recapture studies, which can only be explained by maximum dispersal distances at least twice as large as previously accepted. However, we also find evidence that gaps between sites with suitable habitat exceeding ∼ 20 km induce genetic erosion that can be detected from bottleneck analyses. Although further work is needed, our results suggest that M. arion can maintain fully functional metapopulations when they consist of optimal habitat patches that are no further apart than ∼10 km. AU - Ugelvig, Line V AU - Andersen, Anne AU - Boomsma, Jacobus AU - Nash, David ID - 3156 IS - 13 JF - Molecular Ecology TI - Dispersal and gene flow in the rare parasitic Large Blue butterfly Maculinea arion VL - 21 ER - TY - JOUR AB - 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”). AU - Konrad, Matthias AU - Vyleta, Meghan AU - Theis, Fabian AU - Stock, Miriam AU - Tragust, Simon AU - Klatt, Martina AU - Drescher, Verena AU - Marr, Carsten AU - Ugelvig, Line V AU - Cremer, Sylvia ID - 3242 IS - 4 JF - PLoS Biology TI - Social transfer of pathogenic fungus promotes active immunisation in ant colonies VL - 10 ER - TY - GEN AB - 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”). AU - Konrad, Matthias AU - Vyleta, Meghan AU - Theis, Fabian AU - Stock, Miriam AU - Klatt, Martina AU - Drescher, Verena AU - Marr, Carsten AU - Ugelvig, Line V AU - Cremer, Sylvia ID - 9755 TI - Data from: Social transfer of pathogenic fungus promotes active immunisation in ant colonies ER - TY - GEN AB - 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. AU - Tragust, Simon AU - Mitteregger, Barbara AU - Barone, Vanessa AU - Konrad, Matthias AU - Ugelvig, Line V AU - Cremer, Sylvia ID - 9757 TI - Data from: Ants disinfect fungus-exposed brood by oral uptake and spread of their poison ER - TY - JOUR AB - Background: Fragmentation of terrestrial ecosystems has had detrimental effects on metapopulations of habitat specialists. Maculinea butterflies have been particularly affected because of their specialized lifecycles, requiring both specific food-plants and host-ants. However, the interaction between dispersal, effective population size, and long-term genetic erosion of these endangered butterflies remains unknown. Using non-destructive sampling, we investigated the genetic diversity of the last extant population of M. arion in Denmark, which experienced critically low numbers in the 1980s. Results: Using nine microsatellite markers, we show that the population is genetically impoverished compared to nearby populations in Sweden, but less so than monitoring programs suggested. Ten additional short repeat microsatellites were used to reconstruct changes in genetic diversity and population structure over the last 77 years from museum specimens. We also tested amplification efficiency in such historical samples as a function of repeat length and sample age. Low population numbers in the 1980s did not affect genetic diversity, but considerable turnover of alleles has characterized this population throughout the time-span of our analysis. Conclusions: Our results suggest that M. arion is less sensitive to genetic erosion via population bottlenecks than previously thought, and that managing clusters of high quality habitat may be key for long-term conservation. AU - Ugelvig, Line V AU - Nielsen, Per AU - Boomsma, Jacobus AU - Nash, David ID - 3388 IS - 201 JF - BMC Evolutionary Biology TI - Reconstructing eight decades of genetic variation in an isolated Danish population of the large blue butterfly Maculinea arion VL - 11 ER - TY - JOUR AB - Evolutionary theories of ageing predict that life span increases with decreasing extrinsic mortality, and life span variation among queens in ant species seems to corroborate this prediction: queens, which are the only reproductive in a colony, live much longer than queens in multi-queen colonies. The latter often inhabit ephemeral nest sites and accordingly are assumed to experience a higher mortality risk. Yet, all prior studies compared queens from different single- and multi-queen species. Here, we demonstrate an effect of queen number on longevity and fecundity within a single, socially plastic species, where queens experience the similar level of extrinsic mortality. Queens from single- and two-queen colonies had significantly longer lifespan and higher fecundity than queens living in associations of eight queens. As queens also differ neither in morphology nor the mode of colony foundation, our study shows that the social environment itself strongly affects ageing rate. AU - Schrempf, Alexandra AU - Cremer, Sylvia AU - Heinze, Jürgen ID - 3386 IS - 7 JF - Journal of Evolutionary Biology TI - Social influence on age and reproduction reduced lifespan and fecundity in multi queen ant colonies VL - 24 ER - TY - JOUR AB - Context-dependent adjustment of mating tactics can drastically increase the mating success of behaviourally flexible animals. We used the ant Cardiocondyla obscurior as a model system to study adaptive adjustment of male mating tactics. This species shows a male diphenism of wingless fighter males and peaceful winged males. Whereas the wingless males stay and exclusively mate in the maternal colony, the mating behaviour of winged males is plastic. They copulate with female sexuals in their natal nests early in life but later disperse in search for sexuals outside. In this study, we observed the nest-leaving behaviour of winged males under different conditions and found that they adaptively adjust the timing of their dispersal to the availability of mating partners, as well as the presence, and even the type of competitors in their natal nests. In colonies with virgin female queens winged males stayed longest when they were the only male in the nest. They left earlier when mating partners were not available or when other males were present. In the presence of wingless, locally mating fighter males, winged males dispersed earlier than in the presence of docile, winged competitors. This suggests that C. obscurior males are capable of estimating their local breeding chances and adaptively adjust their dispersal behaviour in both an opportunistic and a risk-sensitive way, thus showing hitherto unknown behavioural plasticity in social insect males. AU - Cremer, Sylvia AU - Schrempf, Alexandra AU - Heinze, Jürgen ID - 3399 IS - 3 JF - PLoS One TI - Competition and opportunity shape the reproductive tactics of males in the ant Cardiocondyla obscurior VL - 6 ER -