Survival after pathogen exposure in group‐living insects: don't forget the stress of social isolation!

A major cost of group‐living is its inherent risk of pathogen infection. To limit this risk, many group‐living animals have developed the capability to prophylactically boost their immune system in the presence of group members and/or to mount collective defences against pathogens. These two phenomena, called density‐dependent prophylaxis and social immunity, respectively, are often used to explain why, in group‐living species, individuals survive better in groups than in isolation. However, this survival difference may also reflect an alternative and often overlooked process: a cost of social isolation on individuals’ capability to fight against infections. Here, we disentangled the effects of density‐dependent prophylaxis, social immunity and stress of social isolation on the survival after pathogen exposure in group‐living adults of the European earwig Forficula auricularia. By manipulating the presence of group members both before and after pathogen exposure, we demonstrated that the cost of being isolated after infection, but not the benefits of social immunity or density‐dependent prophylaxis, explained the survival of females. Specifically, females kept constantly in groups or constantly isolated had higher survival rates than females that were first in groups and then isolated after infection. Our results also showed that this cost of social isolation was absent in males and that social isolation did not reduce the survival of noninfected individuals. Overall, this study gives a new perspective on the role of pathogens in social evolution, as it suggests that an apparently nonadaptive, personal immune process may promote the maintenance of group‐living under pathogenic environments.     

Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis

In primitively eusocial insects, caste expression is flexible. Even though Polistes species are well known to show social trait variation (e.g., worker vs. gyne) depending on ecological context, loss of worker caste in some populations of a eusocial, worker-containing species has never been documented. We report first data on geographic variation in caste expression in Polistes biglumis. We compared physiological and behavioural traits of the first female offspring from four populations that experience different climatic conditions and social parasite prevalence. We demonstrated that the first female offspring to emerge in cold areas with high parasite prevalence had more abundant, gyne-like fat bodies and exhibited lower foraging effort, in comparison to the first female offspring produced in warm areas with low parasite prevalence. Thus, the populations under severe environmental conditions produced a totipotent female offspring and suppressed worker production, whereas the population living in less extreme environmental conditions produced worker-like females as first female offspring and gyne-like females as offspring that emerged later. The existence of mixed social strategies among populations of primitively eusocial species could have important consequences for the study of social evolution, shedding light on the sequence of steps by which populations evolve between the extremes of solitary state and eusocial state.     

From individual to collective immunity: the role of the venom as antimicrobial agent in the Stenogastrinae wasp societies

Sociality is associated with an increased risk of disease transmission and one of the first defense of the insect colonies is represented by antimicrobial secretions. In many eusocial hymenopteran species venom glands represent one of the most important source of antimicrobial substances. It is known that in highly eusocial species the venom is spread on both the cuticle of insects and the comb, thus becoming a component of the so called "social immunity". So far, it is never been ascertained whether this phenomenon is also present in more primitively eusocial and incipiently eusocial groups. Using incipiently eusocial hover wasps as model, we demonstrate that venom is present on insect cuticles and that it strongly acts against microorganisms. By contrast, the nest, regardless of materials, does not represent a 'medium" where the venom is deposited by wasps in order to act as a social antiseptic weapon. Our findings discussed in an evolutionary perspective indicate that a certain degree of sociality or a sufficient number of individuals in an insect society are thresholds to be reached for the rise of complex and efficient forms of collective and social immunity as mechanisms of resistance to diseases.     

Social immunity

Social insect colonies have evolved collective immune defences against parasites. These 'social immune systems' result from the cooperation of the individual group members to combat the increased risk of disease transmission that arises from sociality and group living. In this review we illustrate the pathways that parasites can take to infect a social insect colony and use these pathways as a framework to predict colony defence mechanisms and present the existing evidence. We find that the collective defences can be both prophylactic and activated on demand and consist of behavioural, physiological and organisational adaptations of the colony that prevent parasite entrance, establishment and spread. We discuss the regulation of collective immunity, which requires complex integration of information about both the parasites and the internal status of the insect colony. Our review concludes with an examination of the evolution of social immunity, which is based on the consequences of selection at both the individual and the colony level.     

Population genomics of eusocial insects: the costs of a vertebrate‐like effective population size

The evolution of reproductive division of labour and social life in social insects has lead to the emergence of several life‐history traits and adaptations typical of larger organisms: social insect colonies can reach masses of several kilograms, they start reproducing only when they are several years old, and can live for decades. These features and the monopolization of reproduction by only one or few individuals in a colony should affect molecular evolution by reducing the effective population size. We tested this prediction by analysing genome‐wide patterns of coding sequence polymorphism and divergence in eusocial vs. noneusocial insects based on newly generated RNA‐seq data. We report very low amounts of genetic polymorphism and an elevated ratio of nonsynonymous to synonymous changes – a marker of the effective population size – in four distinct species of eusocial insects, which were more similar to vertebrates than to solitary insects regarding molecular evolutionary processes. Moreover, the ratio of nonsynonymous to synonymous substitutions was positively correlated with the level of social complexity across ant species. These results are fully consistent with the hypothesis of a reduced effective population size and an increased genetic load in eusocial insects, indicating that the evolution of social life has important consequences at both the genomic and population levels.     

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

Geographic patterns in the distribution of social systems in terrestrial arthropods

The role of ecology in the evolution and maintenance of arthropod sociality has received increasing research attention in recent years. In some organisms, such as halictine bees, polistine wasps, and social spiders, researchers are investigating the environmental factors that may contribute to high levels of variation in the degree of sociality exhibited both among and within species. Within lineages that include only eusocial members, such as ants and termites, studies focus more on identifying extrinsic factors that may contribute to the dramatic variation in colony size, number of queens, and division of labour that is evident across these species. In this review, I propose a comparative approach that seeks to identify environmental factors that may have a common influence across such divergent social arthropod groups. I suggest that seeking common biogeographic patterns in the distribution of social systems or key social traits may help us to identify ecological factors that play a common role in shaping the evolution of sociality across different organisms. I first review previous studies of social gradients that form along latitudinal and altitudinal axes. Within families and within species, many organisms show an increasing degree of sociality at lower latitudes and altitudes. In a smaller number of cases, organisms form larger groups or found nests cooperatively at higher latitudes and altitudes. I then describe several environmental factors that vary consistently along such gradients, including climate variables and abundance of predators, and outline their proposed role in the social systems of terrestrial arthropods. Finally, I map distributions of a social trait against several climatic factors in five case studies to demonstrate how future comparative studies could inform empirical research.     

Antimicrobial strength increases with group size: implications for social evolution

We hypothesize that aggregations of animals are likely to attract pathogenic micro-organisms and that this is especially the case for semisocial and eusocial insects where selection ultimately led to group sizes in the thousands or even millions, attracting the epithet 'superorganism'. Here, we analyse antimicrobial strength, per individual, in eight thrips species (Insecta: Thysanoptera) that present increasing innate group sizes and show that species with the largest group size (100-700) had the strongest antimicrobials, those with smaller groups (10-80) had lower antimicrobial activity, while solitary species showed none. Species with large innate group sizes showed strong antimicrobial activity while the semisocial species showed no activity until group size increased sufficiently to make activity detectable. The eusocial species behaved in a similar way, with detectable activity appearing once group size exceeded 120. These analyses show that antimicrobial strength is determined by innate group size. This suggests that the evolution of sociality that, by definition, increases group size, may have had particular requirements for defences against microbial pathogens. Thus, increase in group size, accompanied by increased antibiotic strength, may have been a critical factor determining the 'point of no return', early in the evolution of social insects, beyond which the evolution of social anatomical and morphological traits was irreversible. Our data suggest that traits that increase group size in general are accompanied by increased antimicrobial strength and that this was critical for transitions from solitary to social and eusocial organization.     

Fine-scale population structure, inbreeding risk and avoidance in a wild insect population

The ecological and evolutionary importance of fine-scale genetic structure within populations is increasingly appreciated. However, available data are largely restricted to wild vertebrates and eusocial insects. In addition, there is the expectation that most insects tend to have such large- and high-density populations and are so mobile that they are unlikely to face inbreeding risks through fine-scale population structuring. This has made the growing body of evidence for inbreeding avoidance in insects and its implication in mating systems evolution somewhat enigmatic. We present a 4-year study of a natural population of field crickets. Using detailed video monitoring combined with genotyping, we track the movement of all adults within the population and investigate genetic structure at a fine scale. We find some evidence for relatives being found in closer proximity, both across generations and within a single breeding season. Whilst incestuous matings are not avoided, population inbreeding is low, suggesting that mating is close to random and the limited fine-scale structure does not create significant inbreeding risk. Hence, there is little evidence for selective pressures associated with the evolution of inbreeding avoidance mechanisms in a closely related species.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

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.     

Primordial Enemies: Fungal Pathogens in Thrips Societies

Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general?     

Origin and evolution of eusociality: a perspective from studying primitively eusocial wasps

Eusocial insects are those that show overlap of generations, cooperative brood care and reproductive caste differentiation. Of these, primitively eusocial insects show no morphological differences between reproductive and worker castes and exhibit considerable flexibility in the social roles that adult females may adopt. This makes them attractive model systems for investigations concerning the origin of eusociality. The rapidly accumulating information on primitively eusocial wasps suggests that haplodiploidy is unlikely to have an important role in the origin of eusociality. General kin selection (without help from haplodiploidy) could however have been an important factor due to the many advantages of group living. Pre-imaginal caste bias leading to variations in fertility is also likely to have some role. Because workers often have some chance of becoming reproductives in future, mutualism and other individual selection models suggest themselves as important factors. A hypothesis for the route to eusociality which focuses on the factors selecting for group living at different stages in social evolution is presented. It is argued that group living originates owing to the benefit of mutualism (the ‘Gambling Stage’) but parental manipulation and subfertility soon become important (the ‘Manipulation Stage’) and finally the highly eusocial state is maintained because genetic asymmetries created by haplodiploidy are exploited by kin recognition (the ‘Recognition Stage’).     

果蝇抗微生物肽基因的免疫诱导模式

果蝇作为一种模式昆虫,为研究昆虫和人类的先天免疫发挥了重要作用。目前对果蝇体内免疫诱导产生的抗微生物肽多基因家族在分子进化、抗菌功能的分子特征和免疫诱导表达的信号传递机制等方面的研究进展,进一步加深了人们对昆虫乃至其他动物和人类先天免疫模式的认识,为研究其他昆虫特别是作为主要农林害虫的鳞翅目昆虫的先天免疫机制发挥了重要作用。本文集中对黑腹果蝇Drosophila melanogaster抗微生物肽及其免疫模式的研究结果和最新进展进行了介绍,其中包括作者近几年的研究结果。     

Convergent evolution in social swallows (Aves: Hirundinidae)

Behavioral shifts can initiate morphological evolution by pushing lineages into new adaptive zones. This has primarily been examined in ecological behaviors, such as foraging, but social behaviors may also alter morphology. Swallows and martins (Hirundinidae) are aerial insectivores that exhibit a range of social behaviors, from solitary to colonial breeding and foraging. Using a well‐resolved phylogenetic tree, a database of social behaviors, and morphological measurements, we ask how shifts from solitary to social breeding and foraging have affected morphological evolution in the Hirundinidae. Using a threshold model of discrete state evolution, we find that shifts in both breeding and foraging social behavior are common across the phylogeny of swallows. Solitary swallows have highly variable morphology, while social swallows show much less absolute variance in all morphological traits. Metrics of convergence based on both the trajectory of social lineages through morphospace and the overall morphological distance between social species scaled by their phylogenetic distance indicate strong convergence in social swallows, especially socially foraging swallows. Smaller physical traits generally observed in social species suggest that social species benefit from a distinctive flight style, likely increasing maneuverability and foraging success and reducing in‐flight collisions within large flocks. These results highlight the importance of sociality in species evolution, a link that had previously been examined only in eusocial insects and primates.     

Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae)

We performed a phylogenetic analysis of the species, species groups, and subgenera within the predominantly eusocial lineage of Lasioglossum (the Hemihalictus series) based on three protein coding genes: mitochondrial cytochrome oxidase I, nuclear elongation factor 1alpha and long-wavelength rhodopsin. The entire data set consisted of 3421 aligned nucleotide sites, 854 of which were parsimony informative. Analyses by equal weights parsimony, maximum likelihood, and Bayesian methods yielded good resolution among the 53 taxa/populations, with strong bootstrap support and high posterior probabilities for most nodes. There was no significant incongruence among genes, and parsimony, maximum likelihood, and Bayesian methods yielded congruent results. We mapped social behavior onto the resulting tree for 42 of the taxa/populations to infer the likely history of social evolution within Lasioglossum. Our results indicate that eusociality had a single origin within Lasioglossum. Within the predominantly eusocial clade, however, there have been multiple (six) reversals from eusociality to solitary nesting, social polymorphism, or social parasitism, suggesting that these reversals may be more common in primitively eusocial Hymenoptera than previously anticipated. Our results support the view that eusociality is hard to evolve but easily lost. This conclusion is potentially important for understanding the early evolution of the advanced eusocial insects, such as ants, termites, and corbiculate bees.     

Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.     

Medium molecular weight polar substances of the cuticle as tools in the study of the taxonomy,systematics and chemical ecology of tropical hover wasps (Hymenoptera: Stenogastrinae)

The Stenogastrinae wasps have been proposed as a key group for an understanding of social evolution in insects, but the phylogeny of the group is still under discussion. The use of chemical characters, in particular cuticular hydrocarbons, for insect taxonomy is relatively recent and only a few studies have been conducted on the cuticular polar substances. In this work, we ascertain, by the matrix‐assisted laser desorption ionization‐time of flight mass spectrometry technique, that different species of primitively eusocial hover wasps have different compositions of the epicuticular polar compounds ranging from 900 to 3600 Da. General linear model analysis and discriminant analysis showed that the average spectral profiles of this fraction can be diagnostic for identification of the species. Moreover, for the first time we show population diversification in the medium MW polar cuticular mixtures in insects. In conclusion, the results demonstrate that the chemical characters are consistent with the physical characters and the study support the importance of medium MW polar substances as powerful tools for systematics (chemosystematics) and chemical ecology (fertility signal and population characterization) in a primitively social insect taxon.