Social immunity in honeybees—Density dependence,diet, and body mass trade‐offs

Group living is favorable to pathogen spread due to the increased risk of disease transmission among individuals. Similar to individual immune defenses, social immunity, that is antiparasite defenses mounted for the benefit of individuals other than the actor, is predicted to be altered in social groups. The eusocial honey bee (Apis mellifera) secretes glucose oxidase (GOX), an antiseptic enzyme, throughout its colony, thereby providing immune protection to other individuals in the hive. We conducted a laboratory experiment to investigate the effects of group density on social immunity, specifically GOX activity, body mass and feeding behavior in caged honey bees. Individual honeybees caged in a low group density displayed increased GOX activity relative to those kept at a high group density. In addition, we provided evidence for a trade‐off between GOX activity and body mass: Individuals caged in the low group density had a lower body mass, despite consuming more food overall. Our results provide the first experimental evidence that group density affects a social immune response in a eusocial insect. Moreover, we showed that the previously reported trade‐off between immunity and body mass extends to social immunity. GOX production appears to be costly for individuals, and potentially the colony, given that low body mass is correlated with small foraging ranges in bees. At high group densities, individuals can invest less in social immunity than at low densities, while presumably gaining shared protection from infection. Thus, there is evidence that trade‐offs at the individual level (GOX vs. body mass) can affect colony‐level fitness.     

Analogies in the evolution of individual and social immunity

We compare anti-parasite defences at the level of multicellular organisms and insect societies, and find that selection by parasites at these two organisational levels is often very similar and has created a number of parallel evolutionary solutions in the host's immune response. The defence mechanisms of both individuals and insect colonies start with border defences to prevent parasite intake and are followed by soma defences that prevent the establishment and spread of the parasite between the body's cells or the social insect workers. Lastly, germ line defences are employed to inhibit infection of the reproductive tissue of organisms or the reproductive individuals in colonies. We further find sophisticated self/non-self-recognition systems operating at both levels, which appear to be vital in maintaining the integrity of the body or colony as a reproductive entity. We then expand on the regulation of immune responses and end with a contemplation of how evolution may shape the different immune components, both within and between levels. The aim of this review is to highlight common evolutionary principles acting in disease defence at the level of both individual organisms and societies, thereby linking the fields of physiological and ecological immunology.     

Immune defense in leaf-cutting ants: a cross-fostering approach

To ameliorate the impact of disease, social insects combine individual innate immune defenses with collective social defenses. This implies that there are different levels of selection acting on investment in immunity, each with their own trade-offs. We present the results of a cross-fostering experiment designed to address the influences of genotype and social rearing environment upon individual and social immune defenses. We used a multiply mating leaf-cutting ant, enabling us to test for patriline effects within a colony, as well as cross-colony matriline effects. The worker's father influenced both individual innate immunity (constitutive antibacterial activity) and the size of the metapleural gland, which secretes antimicrobial compounds and functions in individual and social defense, indicating multiple mating could have important consequences for both defense types. However, the primarily social defense, a Pseudonocardia bacteria that helps to control pathogens in the ants' fungus garden, showed a significant colony of origin by rearing environment interaction, whereby ants that acquired the bacteria of a foster colony obtained a less abundant cover of bacteria: one explanation for this pattern would be co-adaptation between host colonies and their vertically transmitted mutualist. These results illustrate the complexity of the selection pressures that affect the expression of multilevel immune defenses.     

Phenotypic variation in male and worker encapsulation response in the bumblebee Bombus terrestris

Abstract.  1. Life-history traits such as immunity are often characterised by the presence of large phenotypic variation, but it often remains unclear how and why this variation is maintained by selection.
2. Here an annual social insect, the bumblebee Bombus terrestris , was used to study variation in encapsulation response of males and workers. Bumblebees are a suitable system to study offspring immunity because they are host to a broad variety of different parasites. Bumblebee males, in particular, have a long lifespan compared with other social insect males and their immunity should therefore be an important element for colony reproductive success.
3. Encapsulation response, which was used here as a measurement for the generalised immune defence capacity of an individual, was found to be a highly variable trait. High levels of worker response correlated with low levels of colony parasitism rates.
4. Encapsulation response was found to be (a) lower in males compared with sister workers, and (b) lower in late-produced cohorts compared with early ones.
5. In colonies with delayed sexual reproduction, males had a lower encapsulation response. Thus, investments into immunity seemed reduced in later male cohorts and those eclosing later in the season, perhaps because males had a shorter expected remaining time to acquire matings. The results presented add further evidence that immune defence is a key variable defining colony fitness in social insects.     

昆虫天然免疫相关基因研究进展

在长期进化过程中,昆虫形成了强大的天然免疫防御系统,即体液免疫和细胞免疫。体液免疫主要包括Toll、IMD和JAK/STAT 3条信号通路,通过信号转导及免疫途径调控免疫相关基因的表达,诱导产生抗菌肽和其他效应分子。细胞免疫由血细胞介导,主要完成对病原物的包裹、吞噬和集结等。近年来,昆虫基因组学快速发展,通过生物信息学等方法从昆虫基因组数据中已鉴定到大量免疫相关基因,对这些基因的研究加深了人们对昆虫天然免疫分子机制的认识和理解。根据基因功能,免疫相关基因分为识别、信号转导、调制器、效应分子、黑化反应、RNA干扰和其他基因等7类,这些基因通过互作来调控体液免疫和细胞免疫。本文对昆虫免疫相关基因的分类、功能及家族进化等方面的研究成果进行总结,并对今后昆虫免疫的研究重点进行了展望,以期为昆虫免疫分子机制的研究及开发新的害虫防治策略提供依据。     

Immune-priming in ant larvae: social immunity does not undermine individual immunity

Social insects deploy numerous strategies against pathogens including behavioural, biochemical and immunological responses. While past research has revealed that adult social insects can generate immunity, few studies have focused on the immune function during an insect''s early life stages. We hypothesized that larvae of the black carpenter ant Camponotus pennsylvanicus vaccinated with heat-killed Serratia marcescens should be less susceptible to a challenge with an active and otherwise lethal dose of the bacterium. We compared the in vivo benefits of prior vaccination of young larvae relative to naive and ringer injected controls. Regardless of colony of origin, survival parameters of vaccinated individuals following a challenge were significantly higher than those of the other two treatments. Results support the hypothesis that ant larvae exhibit immune-priming. Based on these results, we can infer that brood care by workers does not eliminate the need for individual-level immunological responses. Focusing on these early stages of development within social insect colonies can start addressing the complex dynamics between physiological (individual level) and social (collective) immunity.     

Food-mediated modulation of immunity in a phytophagous insect: An effect of nutrition rather than parasitic contamination

Inherent to the cost of immunity, the immune system itself can exhibit tradeoffs between its arms. Phytophagous insects face a wide range of microbial and eukaryotic parasites, each activating different immune pathways that could compromise the activity of the others. Feeding larvae are primarily exposed to microbes, which growth is controlled by antibiotic secondary metabolites produced by the host plant. The resulting variation in abundance of microbes on plants is expected to differentially stimulate the insect antimicrobial immune defenses. Under the above tradeoff hypothesis, stimulation of the insect antimicrobial defenses is expected to compromise immune activity against eukaryote parasites. In the European grape berry moth, Eupoecilia ambiguella, immune effectors directed towards microbes are negatively correlated to those directed towards eukaryotic parasites among host plants. Here, we hypothesize this relationship is caused by a variable control of the microbial community among host plants by their antibiotic metabolites. To test this hypothesis, we first quantified antimicrobial activity in berries of several grape varieties. We then measured immune defenses of E. ambiguella larvae raised on artificial diets in which we mimicked levels of antimicrobial activity of grape berries using tetracycline to control the abundance of growing microbes. Another group of larvae was raised on artificial diets made of berry extracts only to control for the effect of nutrition. We found that controlling microbe abundance with tetracycline in diets did not explain variation in the immune function whereas the presence of berry extracts did. This suggests that variation in immune defenses of E. ambiguella among grape varieties is caused by nutritional difference among host plants rather than microbe abundance. Further study of the effects of berry compounds on larval immune parameters will be needed to explain the observed tradeoff among immune system components.     

The biological principles of swarm intelligence

The roots of swarm intelligence are deeply embedded in the biological study of self-organized behaviors in social insects. From the routing of traffic in telecommunication networks to the design of control algorithms for groups of autonomous robots, the collective behaviors of these animals have inspired many of the foundational works in this emerging research field. For the first issue of this journal dedicated to swarm intelligence, we review the main biological principles that underlie the organization of insects’ colonies. We begin with some reminders about the decentralized nature of such systems and we describe the underlying mechanisms of complex collective behaviors of social insects, from the concept of stigmergy to the theory of self-organization in biological systems. We emphasize in particular the role of interactions and the importance of bifurcations that appear in the collective output of the colony when some of the system’s parameters change. We then propose to categorize the collective behaviors displayed by insect colonies according to four functions that emerge at the level of the colony and that organize its global behavior. Finally, we address the role of modulations of individual behaviors by disturbances (either environmental or internal to the colony) in the overall flexibility of insect colonies. We conclude that future studies about self-organized biological behaviors should investigate such modulations to better understand how insect colonies adapt to uncertain worlds.     

Insect immune responses to nematode parasites

Host innate immunity plays a central role in detecting and eliminating microbial pathogenic infections in both vertebrate and invertebrate animals. Entomopathogenic or insect pathogenic nematodes are of particular importance for the control of insect pests and vectors of pathogens, while insect-borne nematodes cause serious diseases in humans. Recent work has begun to use the power of insect models to investigate host-nematode interactions and uncover host antiparasitic immune reactions. This review describes recent findings on innate immune evasion strategies of parasitic nematodes and host cellular and humoral responses to the infection. Such information can be used to model diseases caused by human parasitic nematodes and provide clues indicating directions for research into the interplay between vector insects and their invading tropical parasites.     

Social immunity and the evolution of group living in insects

The evolution of group living requires that individuals limit the inherent risks of parasite infection. To this end, group living insects have developed a unique capability of mounting collective anti-parasite defences, such as allogrooming and corpse removal from the nest. Over the last 20 years, this phenomenon (called social immunity) was mostly studied in eusocial insects, with results emphasizing its importance in derived social systems. However, the role of social immunity in the early evolution of group living remains unclear. Here, I investigate this topic by first presenting the definitions of social immunity and discussing their applications across social systems. I then provide an up-to-date appraisal of the collective and individual mechanisms of social immunity described in eusocial insects and show that they have counterparts in non-eusocial species and even solitary species. Finally, I review evidence demonstrating that the increased risks of parasite infection in group living species may both decrease and increase the level of personal immunity, and discuss how the expression of social immunity could drive these opposite effects. By highlighting similarities and differences of social immunity across social systems, this review emphasizes the potential importance of this phenomenon in the early evolution of the multiple forms of group living in insects.     

Costs of resistance: genetic correlations and potential trade-offs in an insect immune system

Theory predicts that natural selection will erode additive genetic variation in fitness-related traits. However, numerous studies have found considerable heritable variation in traits related to immune function, which should be closely linked to fitness. This could be due to trade-offs maintaining variation in these traits. We used the Egyptian cotton leafworm, Spodoptera littoralis, as a model system to examine the quantitative genetics of insect immune function. We estimated the heritabilities of several different measures of innate immunity and the genetic correlations between these immune traits and a number of life history traits. Our results provide the first evidence for a potential genetic trade-off within the insect immune system, with antibacterial activity (lysozyme-like) exhibiting a significant negative genetic correlation with haemocyte density, which itself is positively genetically correlated with both haemolymph phenoloxidase activity and cuticular melanization. We speculate on a potential trade-off between defence against parasites and predators, mediated by larval colour, and its role in maintaining genetic variation in traits under natural selection.     

Introduction. Ecological immunology

An organism's fitness is critically reliant on its immune system to provide protection against parasites and pathogens. The structure of even simple immune systems is surprisingly complex and clearly will have been moulded by the organism's ecology. The aim of this review and the theme issue is to examine the role of different ecological factors on the evolution of immunity. Here, we will provide a general framework of the field by contextualizing the main ecological factors, including interactions with parasites, other types of biotic as well as abiotic interactions, intraspecific selective constraints (life-history trade-offs, sexual selection) and population genetic processes. We then elaborate the resulting immunological consequences such as the diversity of defence mechanisms (e.g. avoidance behaviour, resistance, tolerance), redundancy and protection against immunopathology, life-history integration of the immune response and shared immunity within a community (e.g. social immunity and microbiota-mediated protection). Our review summarizes the concepts of current importance and directs the reader to promising future research avenues that will deepen our understanding of the defence against parasites and pathogens.     

Regulators and signalling in insect antimicrobial innate immunity: Functional molecules and cellular pathways

Insects possess an immune system that protects them from attacks by various pathogenic microorganisms that would otherwise threaten their survival. Immune mechanisms may deal directly with the pathogens by eliminating them from the host organism or disarm them by suppressing the synthesis of toxins and virulence factors that promote the invasion and destructive action of the intruder within the host. Insects have been established as outstanding models for studying immune system regulation because innate immunity can be explored as an integrated system at the level of the whole organism. Innate immunity in insects consists of basal immunity that controls the constitutive synthesis of effector molecules such as antimicrobial peptides, and inducible immunity that is activated after detection of a microbe or its product(s). Activation and coordination of innate immune defenses in insects involve evolutionary conserved immune factors. Previous research in insects has led to the identification and characterization of distinct immune signalling pathways that modulate the response to microbial infections. This work has not only advanced the field of insect immunology, but it has also rekindled interest in the innate immune system of mammals. Here we review the current knowledge on key molecular components of insect immunity and discuss the opportunities they present for confronting infectious diseases in humans.     

Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity

Insects transmit the causative agents for such debilitating diseases as malaria, lymphatic filariases, sleeping sickness, Chagas' disease, leishmaniasis, river blindness, Dengue, and yellow fever. The persistence of these diseases provides testimony to the genetic capacity of parasites to evolve strategies that ensure their successful development in two genetically diverse host species: insects and mammals. Current efforts to address the problems posed by insect-borne diseases benefit from a growing understanding of insect and mammalian immunity. Of considerable interest are recent genomic investigations that show several similarities in the innate immune effector responses and associated regulatory mechanisms manifested by insects and mammals. One notable exception, however, is the nearly universal presence of a brown-black pigment accompanying cellular innate immunity in insects. This response, which is unique to arthropods and certain other invertebrates, has focused attention on the elements involved in pigment synthesis as causing or contributing to the death of the parasite, and has even prompted speculation that the enzyme cascade mediating melanogenesis constitutes an ill-defined recognition mechanism. Experimental evidence defining the role of melanin and its precursors in insect innate immunity is severely lacking. A great deal of what is known about melanogenesis comes from studies of the process occurring in mammalian systems, where the pigment is synthesized by such diverse cells as those comprising portions of the skin, hair, inner ear, brain, and retinal epithelium. Fortunately, many of the components in the metabolic pathways leading to the formation of melanin have been found to be common to both insects and mammals. This review examines some of the factors that influence enzyme-mediated melanogenic responses, and how these responses likely contribute to blood cell-mediated, target-specific cytotoxicity in immune challenged insects.     

How to kill a mocking bug?

All metazoans have evolved means to protect themselves from threats present in the environment: injuries, viruses, fungi, bacteria and other parasites. Insect protection includes innate physical barriers and both cellular and humoral responses. The insect innate immune response, best characterized in Drosophila melanogaster, is a rapid broad response, triggered by pathogen-associated molecular patterns (PAMPs) recognition, which produces a limited range of effectors that does not alter upon continued pathogen exposure and lacks immunological memory. The Drosophila response, particularly its humoral response, has been investigated by both low and high-throughput methods. Three signalling pathways conserved between insects and mammals have been implicated in this response: Toll (equivalent to mammalian TLR), Imd (equivalent to TNFalpha) and Hop (equivalent to JAK/STAT). This review provides an entry point to the insect immune system literature outlining the main themes in D. melanogaster bacterial pathogen detection and humoral and cellular immune responses. The Drosophila immune response is compared with other insects and the mammalian immune system.     

Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon

Parasites typically reduce host survival or fecundity. To minimize fitness loss, hosts can make temporal adjustments of their reproductive effort. To date such plastic shifts of life‐history traits in response to parasitism are only known from solitary organisms where infected individuals can react by themselves. In the case of social insects, where brood care and reproductive effort is shared between reproductive individuals (typically the queen) and workers, adjustments of the reproductive effort would depend on collective decision‐making. We tested for this possibility by experimentally activating the immune response of individual workers in colonies of the bumblebee, Bombus terrestris L. This induction resulted, in combination with environmental conditions, in a reduction of fitness of the social unity (i.e. colony success, measured by number and biomass of offspring) and a collective response towards earlier reproduction. As both phenomena are expressed at the level of the colony, the result suggests that key elements of the use of immune defence have been maintained through the evolutionary transition to sociality.     

The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group

The collective behaviour of social groups is often strongly influenced by one or few individuals, termed here ‘keystone individuals’. We examined whether the influence of keystone individuals on collective behaviour lingers after their departure and whether these lingering effects scale with their tenure in the group. In the social spider, Stegodyphus dumicola, colonies'' boldest individuals wield a disproportionately large influence over colony behaviour. We experimentally manipulated keystones'' tenure in laboratory-housed colonies and tracked their legacy effects on collective prey capture following their removal. We found that bolder keystones caused more aggressive collective foraging behaviour and catalysed greater inter-individual variation in boldness within their colonies. The longer keystones remained in a colony, the longer both of these effects lingered after their departure. Our data demonstrate that, long after their disappearance, keystones have large and lasting effects on social dynamics at both the individual and colony levels.     

Eicosanoid actions in insect cellular immune functions

Insects are more or less constantly challenged with a daunting array of pathogenic organisms, including viruses, bacteria, fungi, protozoans as well as various metazoan parasites and parasitoids. At the first level of defense, the pathogens are rebuffed by physical barriers, including the cuticle and peritrophic membrane. Upon breaching these barriers, pathogens meet with an arsenal of robust and efficacious immune defense mechanisms. Two general categories of defenses are typically recognized, humoral defenses and hemocytic or cellular defenses. The former involves induced synthesis of various antibacterial proteins and peptides, such as cecropins and lysozyme. Cellular defense mechanisms are characterized by direct interactions between circulating hemocytes and the invaders. These include phagocytosis, microaggregation, nodulation, and encapsulation. Microaggregation is a step in the nodulation process, which is responsible for clearing the bulk of bacterial infections from circulation. Coordinated cellular actions lead to encapsulation of invaders, such as parasitoid eggs, that are very much larger than individual hemocytes. While the defense mechanisms are broadly appreciated, less is known about the biochemical signals responsible for mediating and coordinating the cellular actions. We now know eicosanoids mediate phagocytosis, microaggregation, and nodulation reactions to immune challenge, as well as cell spreading, a specific step in nodulation. We have several goals in this mini review. We provide a brief background on cellular immunity, outline eicosanoid biosynthesis, and review eicosanoid actions in cellular immunity in insects. Recent work indicates some pathogens have usurped eicosanoid‐mediated immunity; they disable insect immunity by inhibiting eicosanoid biosynthesis. We interpret these findings and their significance with respect to the biological control of insects. We also present preliminary work designed to test hypotheses on how eicosanoids exert their actions. We address shortcomings in our knowledge on eicosanoids in insect biology.     

Identification of 3,4-dihydroxyphenylalanine, 5,6-dihydroxyindole, and N-acetylarterenone during eumelanin formation in immune reactive larvae of Drosophila melanogaster.

3,4-Dihydroxyphenylalanine, 5-6-dihydroxyindole, and N-acetylarterenone were detected by electrochemical methods in the hemolymph of immune reactive larvae of Drosophila melanogaster following parasitization by the wasp Leptopilina boulardi. Determinations of the catechols were made after separation by reverse phase, ion-pairing high pressure liquid chromatography with electrochemical detection. The presence of 5,6-dihydroxyindole unequivocally establishes the eumelanin pathway in the defense response of Drosophila, and confirms previous investigations which have implicated certain catecholamine metabolizing enzymes in insect immunity. The occurrence of N-acetylarterenone, a derivative of the principal sclerotizing agent N-acetyldopamine, verifies the existence and proposed involvement of quinone methide isomerase in the regulation of catecholamine metabolism, and suggests that the cellular capsule formed by Drosophila in immune reactions against parasites is most likely a composite of both eumelanin and sclerotin. The absence of 3,4-dihydroxyphenylacetic acid in hemolymph samples from immune reactive hosts suggests that during parasitization certain catecholamines and metabolic precursors may be re-employed in alternate pathways, some of which may be used in defense reactions.