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Infections early in life can have enduring effects on an organism's development and immunity. In this study, we show that this equally applies to developing 'superorganisms'--incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colonies grew more slowly than controls before winter, but reached similar sizes afterwards. Independent of exposure, queen hibernation survival improved when the ratio of pupae to workers was small. Queens that reared fewer pupae before worker emergence exhibited lower pathogen levels, indicating that high brood rearing efforts interfere with the ability of the queen's immune system to suppress pathogen proliferation. Early-life queen pathogen exposure also improved the immunocompetence of her worker offspring, as demonstrated by challenging the workers to the same pathogen a year later. Transgenerational transfer of the queen's pathogen experience to her workforce can hence durably reduce the disease susceptibility of the whole superorganism.

“Ecological intelligence” hypotheses posit that animal learning and memory evolve to meet the demands posed by foraging and, together with social intelligence and cognitive buffer hypotheses, provide a key framework for understanding cognitive evolution.1, 2, 3, 4, 5 However, identifying the critical environments where cognitive investment reaps significant benefits has proved challenging.6, 7, 8 Here, we capitalize upon seasonal variation in forage availability for a social insect model (Bombus terrestris audax) to establish how the benefits of short-term memory, assayed using a radial arm maze (RAM), vary with resource availability. Following a staggered design over 2 years, whereby bees from standardized colonies at identical life-history stages underwent cognitive testing before foraging in the wild, we found that RAM performance predicts foraging efficiency—a key determinant of colony fitness—in plentiful spring foraging conditions but that this relationship is reversed during the summer floral dearth. Our results suggest that the selection for enhanced cognitive abilities is unlikely to be limited to harsh environments where food is hard to find or extract,5,9, 10 highlighting instead that the challenges of rich and plentiful environments, which present multiple options in short succession, could be a broad driver in the evolution of certain cognitive traits.

Summary “Ecological intelligence” hypotheses posit that the benefits of cognitive investment vary with foraging ecology, and provide a key framework for understanding the evolution of animal learning and memory1–4. However, although certain ecological selection pressures have been found to correlate with brain or neural region size5–8, empirical evidence to show that any specific cognitive trait is useful in certain environments but not others is currently lacking. Here, we assay the short-term memory of bumblebee (Bombus terrestris audax) workers from 25 identically reared colonies, before allowing each colony to forage in a landscape where forage availability varies seasonally. Through analysis of the bees’ lifetime foraging careers, comprising >1700 foraging trips over two years, we show that performance on a task designed to test short-term memory predicts individual foraging efficiency – a fitness proxy that is key to colony reproductive output – in plentiful spring foraging conditions. However, this relationship is reversed during the summer floral dearth, when the costs of cognitive investment may outweigh the benefits. Our results provide evidence that the value of a cognitive trait depends upon the prevailing ecological conditions and suggest that temporal changes in that environment could place contrasting selection pressures on memory within a single species.

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.

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.

Social insects colonies protect themselves against pathogens by collectively performing disease defences that result in social immunity. As a first barrier to disease, sanitary care between nestmates reduces individual-level exposure and infection. However, if a pathogen overcomes these defences, social insects should have evolved mechanisms to prevent individual infections causing systemic disease spread in the colony. In this study, we investigated how ants prevent disease outbreaks following the successful infection of their brood with a fungal pathogen. We found that the ants can detect lethal infections early in the non-infectious incubation period of the pathogen9s lifecycle, using chemical "sickness cues" expressed by the infected pupae. Following detection, the pupae are unpacked from their cocoons by the ants and bitten to make perforations in the cuticle, through which the ants spray their antimicrobial poison. Since the cocoon and cuticle act as barriers against the poison, this multicomponent behaviour permits the ants to use their poison for internal disinfection of the pupal body, where it can act directly against the proliferating pathogen. We termed this mechanism destructive disinfection as it killed the pupae and prevented pathogen replication. Ultimately, the ants stopped the pathogen from completing its lifecycle and transmitting to new hosts. Thus, destructive disinfection acts as a second line of defence against disease in ant colonies and is analogous to the elimination of infected cells by adaptive immune systems. Our results therefore suggest that pathogen-induced selection can result in similar solutions to common problems across the different levels of biological organisation.

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 roles 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.

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 micro-infections that do not cause disease, but still affect host immunity by either decreasing or increasing the host’s vulnerability to subsequent pathogen 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 here tested if the altered disease susceptibility of experienced caregivers, in turn, affects their expression of sanitary care behaviour. We found that micro-infections contracted during sanitary care had protective or neutral effects upon secondary exposure to the same (homologous) pathogen, but consistently induced high mortality upon super-infection 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 yet more antimicrobial disinfection, when caring for nestmates contaminated with heterologous pathogens as compared to homologous ones. By modulating the components of sanitary care in this way, the ants reduced their probability of contracting super-infections of the harmful heterologous pathogens. 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.

Summary 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.

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.

Systemic insecticides such as neonicotinoids and sulfoximines can be present in the nectar and pollen of treated crops, through which foraging bees can become acutely exposed. Research has shown that acute, field realistic dosages of neonicotinoids can negatively influence bee learning and memory, with potential consequences for bee behaviour. As legislative reassessment of neonicotinoid use occurs globally, there is an urgent need to understand the potential risk of other systemic insecticides. Sulfoxaflor, the first branded sulfoximine-based insecticide, has the same mode of action as neonicotinoids, and may potentially replace them over large geographical ranges. Here we assessed the impact of acute sulfoxaflor exposure on performance in two paradigms that have previously been used to illustrate negative impacts of neonicotinoid pesticides on bee learning and memory. We assayed whether acute sulfoxaflor exposure influences (a) olfactory conditioning performance in both bumblebees (Bombus terrestris) and honeybees (Apis mellifera), using a proboscis extension reflex assay, and (b) working memory performance of bumblebees, using a radial-arm maze. We found no evidence to suggest that sulfoxaflor influenced performance in either paradigm. Our results suggest that despite a shared mode of action between sulfoxaflor and neonicotinoid-based insecticides, widely-documented effects of neonicotinoids on bee cognition may not be observed with sulfoxaflor, at least at acute exposure regimes.