Social Insects Research Articles

High Nutritional Conditions Influence Feeding Plasticity in Pristionchus pacificus and Render Worms Non-Predatory.

Developmental plasticity, the ability of a genotype to produce different phenotypes in response to environmental conditions, has been subject to intense studies in the last four decades. The self-fertilising nematode Pristionchus pacificus has been developed as a genetic model system for studying developmental plasticity due to its mouth-form polyphenism that results in alternative feeding strategies with a facultative predatory and non-predatory mouth form. Many studies linked molecular aspects of the regulation of mouth-form polyphenism with investigations of its evolutionary and ecological significance. Also, several environmental factors influencing P. pacificus feeding structure expression were identified including temperature, culture condition and population density. However, the nutritional plasticity of the mouth form has never been properly investigated although polyphenisms are known to be influenced by changes in nutritional conditions. For instance, studies in eusocial insects and scarab beetles have provided significant mechanistic insights into the nutritional regulation of polyphenisms but also other forms of plasticity. Here, we study the influence of nutrition on mouth-form polyphenism in P. pacificus through experiments with monosaccharide and fatty acid supplementation. We show that in particular glucose supplementation renders worms non-predatory. Subsequent transcriptomic and mutant analyses indicate that de novo fatty acid synthesis and peroxisomal beta-oxidation pathways play an important role in the mediation of this plastic response. Finally, the analysis of fitness consequences through fecundity counts suggests that non-predatory animals have an advantage over predatory animals grown in the glucose-supplemented condition.

Nylanderia of the World, Part IV: Taxonomic contributions to the American Clade I of New World Nylanderia (Hymenoptera: Formicidae)

Globally, potentially hundreds of Nylanderia species remain undescribed, hidden within several broadly distributed complexes of morphologically cryptic species. By integrating phylogenomics, geography, and morphology, we describe eight new Nylanderia species from southern Mexico and Mesoamerica, increasing the total number of known species in the genus to 131. In the Americas, Nylanderia is divided into two distantly related clades: American Clade I (AC1) and American Clade II (AC2). Within AC1, Nylanderia austroccidua (Trager) was originally described as a widespread and morphologically variable species distributed from Utah to Costa Rica. This species was diagnosed by a slight concavity in the anterior face of the pronotum and varying degrees of fine cuticular microsculpturing across the body that causes blue cuticular iridescence under microscopic examination. Using Ultraconserved Elements (UCEs) for molecular phylogenetic analysis, we found that taxa matching the original description of N. austroccidua are paraphyletic with respect to Nearctic Nylanderia species. We also found that AC1 includes a Neotropical subclade extending into Mesoamerica, the distribution of which overlaps with AC2, which is exclusively Neotropical. Along with an updated description of N. austroccidua, we also describe the following new species belonging to clade AC1: N. breviscapa, sp. nov., N. contraria, sp. nov., N. lazulina, sp. nov., N. luceata, sp. nov., N. mendax sp. nov., N. mosaica sp. nov., N. polita sp. nov., and N. usul, sp. nov. A dichotomous key and images of the worker caste of these species are included and, where available, images of queens and males are provided.

Evaluating UCE Data Adequacy and Integrating Uncertainty in a Comprehensive Phylogeny of Ants.

While some relationships in phylogenomic studies have remained stable since the Sanger sequencing era, many challenging nodes remain, even with genome-scale data. Incongruence or lack of resolution in the phylogenomic era is frequently attributed to inadequate data modeling and analytical issues that lead to systematic biases. However, few studies investigate the potential for random error or establish expectations for the level of resolution achievable with a given empirical dataset and integrate uncertainties across methods when faced with conflicting results. Ants are the most species-rich lineage of social insects and one of the most ecologically important terrestrial animals. Consequently, ants have garnered significant research attention, including their systematics. Despite this, there has been no comprehensive genus-level phylogeny of the ants inferred using genomic data that thoroughly evaluates both signal strength and incongruence. In this study, we provide insight into and quantify uncertainty across the ant tree of life by utilizing the most taxonomically comprehensive Ultraconserved Elements dataset of ants to date, including 277 (81%) of recognized ant genera from all 16 extant subfamilies, and representing over 98% of described species. We use simulations to establish expectations for resolution, identify branches with less-than-expected concordance, and dissect the effects of data and model selection on recalcitrant nodes. Simulations show that hundreds of loci are needed to resolve recalcitrant nodes on our genus-level ant phylogeny. This demonstrates the continued role of random error in phylogenomic studies. Our analyses provide a comprehensive picture of support and incongruence across the ant phylogeny, while offering a more nuanced depiction of uncertainty and significantly expanding generic sampling. We use a consensus approach to integrate uncertainty across different analyses and find that assumptions about root age exert substantial influence on divergence dating. Our results suggest that advancing the understanding of ant phylogeny will require not only more data but also more refined phylogenetic models. We also provide a workflow for identifying under-supported nodes in concatenation analyses, outline a pragmatic way to reconcile conflicting results in phylogenomics, and introduce a user-friendly locus selection tool for divergence dating.

Molecular Adjustment to a Social Niche: Brain Transcriptomes Reveal Divergent Influence of Social Environment on the Two Queen Morphs of the Ant Temnothorax rugatulus.

Social insects form complex societies with division of labour between different female castes. In most species, a single queen heads the colony; in others, several queens share the task of reproduction. These different social organisations are often associated with distinct queen morphologies and life-history strategies and occur in different environments. In the ant Temnothorax rugatulus, queens are dimorphic. Macrogynes and microgynes reside in mono- and polygynous colonies and at lower and higher elevations, respectively. We analysed plastic changes in brain transcriptomes in response to the social environment in these queen morphs and their workers. We manipulated the number of queens over 4 months to investigate whether transcriptional activity is influenced by queen morph, social environment or their interaction. Changes in gene expression in the queens' brains in response to our manipulations were largely influenced by the interaction between social environment and queen morph, rather than independently by these factors. Macrogynes and microgynes thus adjust differently to their social environment. Similarly, worker transcriptomes were influenced by an interaction between behavioural type, that is, nurses or foragers, and queen morph. Nurses differentially regulated genes related to nutrition depending on queen morph, suggesting a link between social environment and metabolic dynamics in ant colonies. Overall, our study sheds light on how the social environment influences the molecular physiology of social insects. Furthermore, we demonstrate that in this ant with two queen morphs, worker physiology depends on queen morph and their role in the colony.

Local and landscape factors differently influence health and pollination services in two important pollinator groups.

Agricultural management significantly affects insects, especially pollinators, which are crucial for crop pollination and biodiversity. In agricultural landscapes, various factors spanning different spatial scales are known to affect pollinator health, which, in turn, can influence pollination services. However, the importance of these factors in driving the health and performance of different pollinator groups remains unclear. Using a long-term biodiversity research platform, the German Biodiversity Exploratories, we investigated links between local and landscape-level land-use, health and pollination services in common pollinators, the bumblebee Bombus lapidarius and the syrphid fly Episyrphus balteatus, by measuring various traits as proxies for pollinator health and pollination services. Because of their different life histories, we expected the territorial bumblebees to be more vulnerable to land-use intensification at both spatial levels, compared with the migratory syrphid flies. Both land-use and environmental factors (climate) across spatial scales affected pollinator health, mostly via changes in body size: High land-use intensity reduced bumblebee body size, whereas higher ambient air temperature decreased syrphid fly body size. Increasing proportions of intensively managed areas at the landscape level decreased viral infections in both species. Additionally, landscape-level land-use and climate changed the bumblebees cuticular chemical profile, which is essential for communication in these social insects. Increasing land-use intensity at the local level and higher proportions of intensive land-use at the landscape level both had an indirect negative effect on pollination services in bumblebees via local flower cover and body size. Pollination services in both species were linked to body size. Thus, land-use factors affect pollinator health differently: bumblebees are more vulnerable to local and landscape-level land-use intensification, while syrphid flies are more resilient potentially due to their higher mobility. As pollinator health affects pollination services, our results indicate that land-use intensification poses a high risk to crops pollinated by species with small home ranges.

Ontogeny of energy use in harvester ant colonies, and the metabolic expense of colony growth.

In animals, metabolic rates during ontogeny often scale differently from the way they do in cross-species or population comparisons, with near-isometric scaling patterns more often observed during juvenile growth. In multiple social insect taxa, colony metabolic rate scales hypometrically across species or populations at the same developmental stage, but metabolic patterns during ontogeny have not been examined for any social insect species. We performed the first ontogenetic study of social metabolic scaling in harvester ant colonies (Pogonomyrmex californicus) over 3.5 years as they grew from 52 [Formula: see text] 12 to 767 [Formula: see text] 380 workers. Our data reveal iso- and hypermetric metabolic scaling during the first 20 months of growth, transitioning to hypometric scaling (scaling exponent = 0.93) thereafter. We discovered that the fraction of colony as brood has dual effects on colonial metabolic rate. A higher fraction of the colony that is brood decreases colonial metabolic rate because brood has approximately half the mass-specific metabolic rates of adult ants. Conversely, metabolic rate and activity of adult ants increase as this fraction increases. We further developed a nonlinear composition model, which shows that the maximal colony metabolic rate occurs when 29% of the colony mass is brood, suggesting that demographic changes and colony size may interact to drive the metabolic scaling.

Antimicrobial Activity of Compounds Isolated from the Nest Material of Crematogaster rogenhoferi (Mayr) (Hymenoptera: Formicidae).

Ants as social insects live in groups, which increases the risk of contagious diseases. In response to the threat of pathogens, ants have evolved a variety of defense mechanisms, including incorporating antimicrobial chemicals into nest material for nest hygiene. Crematogaster rogenhoferi is an arboreal ant, building its nest using plant tissues. It is still unclear how C. rogenhoferi is protected against pathogens in its nest. Two main chemicals, 2,2'-methylenebis[6-(1,1-dimethylethyl)-4-methyl-phenol] (MP) and lup-20(29)-en-3-one (LP), isolated from nest materials of C. rogenhoferi were used to investigate ants' anti-pathogenic activity against the entomopathogenic fungus Beauveria bassiana and the entomopathogenic bacteria Serratia marcescens. The results showed that MP and LP can inhibit the growth of B. bassiana through direct contact and fumigation. However, neither MP nor LP had any negative effect on S. marcescens growth. Subsequent analysis showed that MP was found in both the abdomen part and the head part of C. rogenhoferi workers, and LP was not detected in C. rogenhoferi workers. Since LP is a common plant secondary metabolite, it is implied that LP may originate from the plant tissue of C. rogenhoferi nest materials. Our results showed that C. rogenhoferi capitalizes on its own antimicrobial chemicals and probably the chemical defenses which have evolved in plants to protect itself against pathogens.

Post-transcriptional regulation of behavior plasticity in social insects.

Social insects often show remarkable behavioral plasticity, which is closely associated with their respective castes. The underpinnings of this plasticity are complex, involving genetic differences among individuals within a colony and regulation of gene expression at multiple levels. Post-transcriptional regulation, which increases the complexity of the transcriptome, plays a crucial role in the multilayer regulatory network that influences social insect behavior. We provide an overview of the impact of three post-transcriptional regulatory processes on the reproductive division of labor and worker division of labor in social insects: alternative splicing, RNA modifications and non-coding RNAs. We also discuss the relationship between post-transcriptional regulation and chromatin modification.

Randomness as a driver of inactivity in social groups.

Social insects, such as ants and bees, are known for their highly efficient and structured colonies. Division of labour, in which each member of the colony has a specific role, is considered to be one major driver of their ecological success. However, empirical evidence has accumulated showing that many workers, sometimes more than half, remain idle in insect societies. Several hypotheses have been put forward to explain these patterns, but none provides a consensual explanation. Task specialisation exploits inter-individual variations, which are mainly influenced by genetic factors beyond the control of the colony. As a result, individuals may also differ in the efficiency with which they perform tasks. In this context, we aimed to test the hypothesis that colonies generate a large number of individuals in order to recruit only the most efficient to perform tasks, at the cost of producing and maintaining a fraction of workers that remain inactive. We developed a model to explore the conditions under which variations in the scaling of workers' production and maintenance costs, along with activity costs, allow colonies to sustain a fraction of inactive workers. We sampled individual performances according to different random distributions in order to simulate the variability associated with worker efficiency. Our results show that the inactivity of part of the workforce can be beneficial for a wide range of parameters if it allows colonies to select the most efficient workers. In decentralised systems such as insect societies, we suggest that inactivity is a by-product of the random processes associated with the generation of individuals whose performance levels cannot be controlled.

Life expectancy in ants explains variation in helpfulness regardless of phylogenetic relatedness

Abstract Rescue behavior aims to free a relative from danger. Ants are particularly known for such helpfulness and, perhaps not coincidentally, also show the highest level of social organization in the animal kingdom, i.e., eusociality. However, even among social species such as ants, there is a huge variation in rescue proneness and little is understood about the underlying causes of this variation. In this study, we explore the relationship between helpfulness in the form of rescue and life expectancy, focusing on 14 ant species with diverse phylogenetic backgrounds. We posit that species with longer worker life expectancies are more prone to engaging in rescue actions. To test this, we assessed worker lifespan in each species and conducted behavioral tests simulating entrapment scenarios involving a nestmate ensnared by an artificial obstacle. Observed behaviors involved contact with the nestmate, digging around it, pulling at its body parts, and biting the entrapping obstacle. Our findings reveal that species with longer worker life expectancies exhibit higher proneness to rescue endangered nestmates, irrespective of phylogenetic relatedness. Furthermore, we found no trace of a phylogenetic signal in the life expectancies or helpfulness of workers belonging to different species. The results underscore the significance of life expectancy as a key factor influencing the likelihood of rescue behavior in ants. This phenomenon warrants further investigation, given the varied physiologies, life histories, and ecologies observed among species. Nevertheless, the impact of life expectancy on behavioral patterns in social insects suggests that this parameter is likely significant across diverse taxa.

Ageing effects of social environments in 'non-social' insects.

It is increasingly clear that social environments have profound impacts on the life histories of 'non-social' animals. However, it is not yet well known how species with varying degrees of sociality respond to different social contexts and whether such effects are sex-specific. To survey the extent to which social environments specifically affect lifespan and ageing in non-social species, we performed a systematic literature review, focusing on invertebrates but excluding eusocial insects. We found 80 studies in which lifespan or ageing parameters were measured in relation to changes in same-sex or opposite-sex exposure, group size or cues thereof. Most of the studies focused on manipulations of adults, often reporting sex differences in lifespan following exposure to the opposite sex. Some studies highlighted the impacts of developmental environments or social partner age on lifespan. Several studies explored potential underlying mechanisms, emphasizing that studies on insects could provide excellent opportunities to interrogate the basis of social effects on ageing. We discuss what these studies can tell us about the social environment as a stressor, or trade-offs in resources prompted by different social contexts. We suggest fruitful avenues for further research of social effects across a wider and more diverse range of taxa.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

EU Social Economy: Means to ending Inequality?

In recent years, the European Union has been facing increasing technological, economic, environmental and social challenges. The issues of strengthening the social economy are becoming increasingly important in an era of instability and uncertainty in the prospects of global development. The subjects of this business model can play a positive role in achieving the UN Sustainable Development Goals, increasing productivity and competitiveness of both individual enterprises and states and their associations through increased solidarity at the territorial and local levels, reducing poverty and inequality. The social economy is designed to create quality jobs, guarantee equal learning opportunities and provide the necessary social services, especially for vulnerable segments of the population, such as migrants, persons with disabilities and unskilled workers. To realise its mission, its enterprises and organisations need to collaborate with public authorities, stakeholders and users capable of finding solutions to collective problems, such as ethical financing and socially responsible banking. This collaboration can give impetus to social inclusion, economic development and territorial cohesion in depressed underdeveloped areas and regions. Today, social indicators in EU countries such as poverty, inequality, long-term and youth unemployment continue to be high, making it difficult to ensure social sustainability. This article analyses EU policies on the social economy as well as its ecosystem in the region.

Time memory in social insects with a special focus on honey bees.

The ability to associate time and location with food sources is an evolutionary advantage for foraging animals. We find highly sophisticated time memory capabilities especially in social insects, which require efficient foraging capabilities for colony provisioning. Honey bees are perfectly suitable to study time memory mechanisms: they possess an elaborated time memory combined with a relatively simple neuronal clock network and a smaller gene set compared with the mouse model organism. This review provides a short overview majorly across insects, which have demonstrated time memory capabilities, with a focus on time-place learning, and describes basic properties as well as state-of-the-art research connecting time memory with the circadian clock at the behavioral, molecular and neuroanatomical level. Despite a long history of research on time memory of honey bees, putative connections between clock and time memory have only recently been identified and imply a rather complex regulation mechanism with multiple signaling pathways.

Synchronized Rhythmic Activity of Ants with Distributed Rest Periods

Synchronization is a prevalent phenomenon in biological systems, including social insects such as ants. Certain ant species exhibit remarkable synchronization of their activities within the nest. To elucidate the underlying mechanisms of this coordinated behavior, we propose an integro-differential equation model that captures the autocatalytic nature of ant activation. Active ants can stimulate inactive individuals, leading to a cascade of arousal. By incorporating a stochastic component to represent variability in rest periods, we explore the conditions necessary for synchronization. Our analysis reveals a critical threshold for fluctuations in rest duration. Exceeding this threshold disrupts synchronization, driving the system towards a stable equilibrium. These findings offer valuable insights into the factors governing ant activity synchronization and highlight the delicate balance between model parameters required to generate rhythmic patterns.

Discrimination Against Non‐Nestmates Functions to Exclude Socially Parasitic Conspecifics in an Ant

ABSTRACTSocial animals utilise various communication methods to organise their societies. In social insects, nestmate discrimination plays a crucial role in regulating colony membership. Counter to this system, socially parasitic species employ diverse behavioural and chemical strategies to bypass their host's detection. In this study, we tested whether such parasitic adaptations could be detected in the incipient stage of social parasitism that is observed as intraspecific phenomena in some social insects. The Japanese parthenogenetic ant Pristomyrmex punctatus harbours a genetically distinct cheater lineage which infiltrates and exploits host colonies. We found that intrusion of this intraspecific social parasite was defended by nestmate discrimination of host colonies without any behavioural strategies specialised in social parasitism. Most of the cheaters were eliminated through aggression by host workers that are typically observed against non‐nestmates, resulting in a low intrusion success rate for the cheaters (6.7%). Our result contrasts with the expectation from interspecific social parasitism but rather resembles the intraspecific counterpart reported in Cape honeybees (Apis mellifera capensis), illustrating the role of nestmate discrimination in defence against the intrusion of intraspecific social parasites.

Wild chimpanzees remember and revisit concealed, underground army ant nest locations throughout multiple years

Chimpanzees use spatiotemporal cognition for fruit foraging by remembering tree locations and fruiting seasons. However, the spatiotemporal cognition behind exploiting other foods has rarely been studied. Here, we investigate whether chimpanzees use memory to exploit concealed, underground army ant nests. We analyse 679 chimpanzee visits to four nests recorded during five years (2018–2022) using camera traps in a savanna habitat. We explore if chimpanzees intentionally revisit nests, study how they detect ants, and assess ant availability and chimpanzee ant consumption. Nests are concealed, scarce, and intermittently reoccupied, yet chimpanzees eat ants frequently. We find that out of 34 identified chimpanzees who visit the nests, 23 revisit at least one. Chimpanzees visit nest sites significantly more often than similar sites without nests. Individuals revisit significantly sooner and inspect significantly longer nests where they have more recently encountered ants. The apes use sight, smell, taste, touch, and probing tools, to detect ants inside nests. We provide the first evidence suggesting that chimpanzees use spatial and episodic-like memory to exploit concealed social insects throughout multiple years. Our results expand our understanding of the cognitive strategies behind chimpanzee insectivory, suggesting it may have played an important role in the evolution of primate spatiotemporal cognition.

Molecular Basis of Eusocial Complexity: The Case of Worker Reproductivity in Bees.

In eusocial insects, the molecular basis of worker reproductivity, including how it changes with eusocial complexity, remains relatively poorly understood. To address this, we used mRNA-seq to isolate genes differentially expressed between ovary-active and ovary-inactive workers in the intermediately eusocial bumblebee Bombus terrestris. By comparisons with data from the advanced eusocial honeybee Apis mellifera, which shows reduced worker reproductivity, we characterized gene expression differences associated with change in worker reproductivity as a function of eusocial complexity. By comparisons with genes associated with queen-worker caste development in B. terrestris larvae, we tested the behavioral-morphological caste homology hypothesis, which proposes co-option of genes influencing reproductive division of labor in adults in morphological caste evolution. We conducted comparisons having isolated genes expressed in B. terrestris worker-laid eggs to remove the potential confound caused by gene expression in eggs. Gene expression differences between the B. terrestris worker phenotypes were mainly in fat body and ovary, not brain. Many genes (86%) more highly expressed in ovary of ovary-active workers were also expressed in worker-laid eggs, confirming egg-expressed genes were potentially confounding. Comparisons across B. terrestris and A. mellifera, and with B. terrestris larvae, returned significant percentage overlaps in differentially expressed genes and/or enriched Gene Ontology terms, suggesting conserved gene functions underpin worker reproductivity as it declines with increasing eusocial complexity and providing support for the behavioral-morphological caste homology hypothesis. Therefore, within bees, both a degree of conserved gene use and gene co-option appear to underlie the molecular basis of worker reproductivity and morphological caste evolution.

Adult brain neurogenesis does not account for behavioral differences between solitary and social bees.

In many taxa, increasing attention is being paid to how group living shapes the expression of brain plasticity and behavioural flexibility. In eusocial insects, the lifelong commitment of workers and queens to a reproductive or non-reproductive caste is accompanied by a loss of behavioural totipotency, and often, by the expression of a limited behavioural repertoire in workers due to their specialisation. On the other hand, individuals of solitary species have a broader behavioural repertoire as they have to perform all the tasks themselves. This raises the question of whether solitary and social insects differ in their levels of brain plasticity. One mechanism found in both invertebrates and vertebrates to contribute to brain plasticity is adult neurogenesis. It is a mechanism by which adult-born neurons are generated, differentiated and functionally integrated in the brain circuits during adulthood. In this study, we compared the solitary bee Osmia bicornis and the eusocial bee Apis mellifera. We focused on the mushroom bodies which are higher-order integration centres in the insect brain. Based on their known behavioural repertoire, our prediction was that both solitary and social bees would exhibit neurogenesis in the brain until the pupal stage, but that this capacity would persist only in adult solitary bees. However, our results do not validate this prediction, as they indicate that no cells are produced in the mushroom bodies or other areas of the adult solitary bee brain.

Social insects: The waxy wonder of symmetry.

A new study demonstrates that honey bee nests and their contents possess front-to-back symmetry, a design characteristic arising from a proximate thermal cue with an ultimate evolutionary benefit.

Exploring immune memory traits in the social immunity of a fungus-growing ant.

The immune system is crucial for organisms to defend against pathogens. Likewise, analogous immune features evolved against similar pressures at the superorganism scale. Upregulating hygiene to the same fungus pathogen is one assumption for convergent immune mechanisms in social insects, although more evidence of immune memory features remains to be confirmed. Here, we assess immune memory traits at the colony level in the leaf-cutting ant Atta sexdens. We exposed their fungus cultivar to both homologous and heterologous challenges with the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana, as well as the mycoantagonistic fungi Fusarium oxysporum and Trichoderma spirale. By measuring ants' behaviours, we evaluated the capacity of A. sexdens: (i) to enhance their collective hygiene, (ii) speed their hygiene in further infections, (iii) how long this capacity lasts in the colonies and (iv) the degree of specificity to increase hygienic responses. Fungus grooming behaviour was enhanced mostly against entomopathogenic fungi, with a trend of faster reactions during homologous challenges. In general, the capacity to elicit such upregulated actions lasted for up to 30 days, but no longer than 60 days. Overall, colonies exhibited a degree of immune specificity, enhancing hygiene only in response to homologous exposures but decreasing it when infected secondarily with a different fungus, indicating flexible social immunity of A. sexdens after immune challenges.