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Social insects have provided some of the clearest insights into the origins and evolution of collective behaviour. Over 20 years ago, Maynard Smith and Szathmáry defined the most complex form of insect social behaviour—superorganismality—among the eight major transitions in evolution that explain the emergence of biological complexity. However, the mechanistic processes underlying the transition from solitary life to superorganismal living in insects remain rather elusive. An overlooked question is whether this major transition arose via incremental or step-wise modes of evolution. We suggest that examination of the molecular processes underpinning different levels of social complexity represented across the major transition from solitary to complex sociality can help address this question. We present a framework for using molecular data to assess to what extent the mechanistic processes that take place in the major transition to complex sociality and superorganismality involve nonlinear (implying step-wise evolution) or linear (implying incremental evolution) changes in the underlying molecular mechanisms. We assess the evidence for these two modes using data from social insects and discuss how this framework can be used to test the generality of molecular patterns and processes across other major transitions. This article is part of a discussion meeting issue ‘Collective behaviour through time’.

Social insect queens and workers represent ideal models with which to understand the expression and regulation of alternative reproductive phenotypes. Most research in this area has focused on the molecular regulation of reproductive castes in obligately social taxa with complex social systems, while relatively few studies have addressed the molecular basis of caste in species in which the division of reproductive labour is more plastic. As a result, it is not clear whether, and to what extent, the mechanisms of caste in species with reproductive plasticity are the same as those that exist at the highest levels of social complexity. To address this knowledge gap, we analyse brain transcriptomic data for non-reproductives and reproductives of the facultatively social hover wasp Liostenogaster flavolineata, a representative of one of the simplest forms of social living. By experimentally manipulating the reproductive ‘queues’ exhibited by social groups of this species, we show that reproductive division of labour in this species is associated with surprisingly distinct transcriptomic signatures, similar to those observed in more complex social taxa; that variation in gene expression among non-reproductives reflects their investment into foraging effort more than their social rank; and that distinct co-expressed gene sets are associated with differential investment into alternative reproductive strategies. These results elucidate robust transcriptomic signals that represent the proximate basis of division of labour at the simplest level of insect sociality, and show these signals to be remarkably similar to those in more derived species.

1. Citizen science is widely used in ecological research. Data verification of citizen collected data continues to be an issue, and confirming accurate species identification reported by citizens can be especially difficult. \ud 2. Here, we determine the efficacy of using remote learning to identify UK social wasp (Vespinae) species. Citizen scientists (N = 559) collected wasps and identified specimens to species level using a series of online videos and support material. \ud 3. A pre-identification and post-identification questionnaire, and a post-identification assessment test, obtained both qualitative and quantitative data for engagement and changes in identification skills. Some (13.5%) of the participants sent their samples in for expert verification of species identification. \ud 4. Self-assessed skill ratings increased from 2.2/5 pre-identification to 3.5/5 post-identification process. Identification accuracy was high, with 85.6% of assessment test images and 96% of the verified specimens being identified correctly. In previous years, face-to-face public ID workshops with expert trainers yielded an identification accuracy of 91.3%. Eighty-seven percent of participants reported enjoying the experience and would take part again. \ud 5. Remote learning of identification skills in non-specialists can produce greater identification accuracy than face-to-face expert-led workshops, with lower resource requirements and enhanced engagement.

Invasive alien species pose a serious threat to the integrity and function of natural ecosystems. Understanding how these invaders alter natural communities is therefore an important aspect in predicting the likely future outcomes of biological invasions. Many studies have documented the consequences of invasive alien species on native community structure, through the displacement and local extinction of native species. However, sampling methods and intensities are rarely standardised across such studies, meaning that it is not clear whether differences in response among native communities to the same invader species are due to biological differences between the invaded regions, or differences in the methodologies used. Here we use a matched sampling methodology to compare the effects of the Argentine ant (Linepithema humile Mayr) on native ant community assemblages in two distinct biogeographical regions that share similar ecologies: Girona (Spain) and Jonkershoek Nature Reserve (South Africa). We found a strong negative association between L. humile presence and native ant species richness within both geographic regions. However, the effects differed between the two study regions: in Girona, a single native ant species (Plagiolepis pygmaea) persisted in invaded sites; by contrast, substantially more native ant species persisted at invaded sites in Jonkershoek Nature Reserve. In addition, in Jonkershoek Nature Reserve, the abundance of certain native species appeared to increase in the presence of L. humile. This study therefore demonstrates the potential variable effects of an invasive species in contrasting locations within different biogeographical regions. Future work should explore the causes of this differential resistance among communities and expand standardised sampling approaches to more invaded zones to further explore how local biotic or abiotic conditions of a region determine the nature and extent of impact of L. humile invasion on native ant communities This work was funded by grants and awards from the Natural Environmental Research Council (NERC) Case Studentship awarded to SS, JB and RN (NE/K007076/1); COST Action TD1209 (ECOST-STSM-TD1209: 070915-062123, 010715-062122, and 160614-046307); and Varley-Gradwell Travelling Fellowship

Social insects are well known for their aggressive (stinging) responses to a nest disturbance. Still, colonies are attacked due to the high-protein brood cached in their nests. Social wasps have evolved a variety of defense mechanisms to exclude predators, including nest construction and coordinated stinging response. Which predatory pressures have shaped the defensive strategies displayed by social wasps to protect their colonies? We reviewed the literature and explored social media to compare direct and indirect (claims and inferences) evidence of predators attacking individuals and colonies of wasps. Individual foraging wasps are predominantly preyed upon by birds and other arthropods, whereas predators on wasp brood vary across subfamilies of Vespidae. Polistinae wasps are predominantly preyed upon by ants and Passeriformes birds, whereas Vespinae are predominantly preyed upon by badgers, bears, and hawks. Ants and hornets are the primary predators of Stenogastrinae colonies. The probability of predation by these five main Orders of predators varies across continents. However, biogeographical variation in prey–predator trends was best predicted by climate (temperate vs. tropical). In social wasps’ evolutionary history, when colonies were small, predation pressure likely came from small mammals, lizards, or birds. As colonies evolved larger size and larger rewards for predators, the increased predation pressure likely selected for more effective defensive responses. Today, primary predators of large wasp colonies seem to be highly adapted to resist or avoid aggressive nest defense, such as large birds and mammals (which were not yet present when eusociality evolved in wasps), and ants.

Phenotypic plasticity, the ability to produce multiple phenotypes from a single genotype, represents an excellent model with which to examine the relationship between gene expression and phenotypes. Analyses of the molecular foundations of phenotypic plasticity are challenging, however, especially in the case of complex social phenotypes. Here we apply a machine learning approach to tackle this challenge by analyzing individual-level gene expression profiles of Polistes dominula paper wasps following the loss of a queen. We find that caste-associated gene expression profiles respond strongly to queen loss, and that this change is partly explained by attributes such as age but occurs even in individuals that appear phenotypically unaffected. These results demonstrate that large changes in gene expression may occur in the absence of outwardly detectable phenotypic changes, resulting here in a socially mediated de-differentiation of individuals at the transcriptomic level but not at the levels of ovarian development or behavior., Connecting genotypes to complex social behaviour is challenging. Taylor et al. use machine learning to show a strong response of caste-associated gene expression to queen loss, wherein individual wasp’s expression profiles become intermediate between queen and worker states, even in the absence of behavioural changes.

The evolution of eusociality requires that individuals forgo some or all their own reproduction to assist the reproduction of others in their group, such as a primary egg-laying queen. A major open question is how genes and genetic pathways sculpt the evolution of eusociality, especially in rudimentary forms of sociality—those with smaller cooperative nests when compared with species such as honeybees that possess large societies. We lack comprehensive comparative studies examining shared patterns and processes across multiple social lineages. Here we examine the mechanisms of molecular convergence across two lineages of bees and wasps exhibiting such rudimentary societies. These societies consist of few individuals and their life histories range from facultative to obligately social. Using six species across four independent origins of sociality, we conduct a comparative meta-analysis of publicly available transcriptomes. Standard methods detected little similarity in patterns of differential gene expression in brain transcriptomes among reproductive and non-reproductive individuals across species. By contrast, both supervised machine learning and consensus co-expression network approaches uncovered sets of genes with conserved expression patterns among reproductive and non-reproductive phenotypes across species. These sets overlap substantially, and may comprise a shared genetic “toolkit” for sociality across the distantly related taxa of bees and wasps and independently evolved lineages of sociality. We also found many lineage-specific genes and co-expression modules associated with social phenotypes and possible signatures of shared life-history traits. These results reveal how taxon-specific molecular mechanisms complement a core toolkit of molecular processes in sculpting traits related to the evolution of eusociality.

Reproductive conflicts are expected in societies where nonbreeding helpers retain the ability to produce offspring. Despite potential competition from reproductively capable nestmates in social wasps, egg laying tends to be monopolised by a single or relatively few queens. Genetic studies on reproductive partitioning in Polistes paper wasps suggest high reproductive skew in the genus. Conflict is thought to be minimal due to nestmate relatedness or the possibility of inheriting a reproductive monopoly on a nest; consequently, there are inclusive fitness opportunities for nonreproductive helpers. However, most studies are limited to temperate wasp species. Given the cosmopolitan distribution of Polistes, genetic data on group conflicts are required for a broader range of tropical species to determine whether these trends apply across climatic zones. We examined female reproductive skew in the Neotropical paper wasp Polistes lanio, genotyping a selection of adults and pupae from established post-emergence nests using single-nucleotide polymorphisms (SNPs). SNP-based pedigree analyses indicate a reproductive monopoly held by a single queen, with queen replacement from natal nestmates and evidence of possible multiple mating. Relatedness between pupal offspring was high (r = 0.71). It is likely that high reproductive skew among females is a founding trait of Polistes societies, conserved among species that have spread into new environments from Indomalayan origins.

Major evolutionary transitions describe how biological complexity arises; e.g. in the evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. A key mechanistic hypothesis for the evolution of division of labour is that a shared set of genes co-opted from a common solitary ancestral ground plan - a so-called genetic toolkit for sociality - regulate insect castes across different levels of social complexity. The vespid wasps represent an excellent system in which to test this. Here, using conventional and machine learning analyses of brain transcriptome data from nine species of vespid wasps, we find evidence of a shared genetic toolkit across species representing different levels of social complexity, with a large suite of genes classifying castes correctly across species. However, we also found evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that were related to level of social complexity, but also life-history traits (e.g. mode of colony founding). Thus, there appear to be shifts in the gene networks regulating social behaviour and rates of gene evolution that are influenced by innovations in both social complexity and life-history. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality, even within a single lineage. Diversity in lineage, social complexity and life-history traits must be taken into account in the quest to uncover the molecular bases of the major transition to sociality.

Biological systems have the capacity to not only build and robustly maintain complex structures but also to rapidly break up and rebuild such structures. Here, using primitive societies of Polistes wasps, we show that both robust specialization and rapid plasticity are emergent properties of multi-scale dynamics. We combine theory with experiments that, after perturbing the social structure by removing the queen, correlate time-resolved multi-omics with video recordings. We show that the queen-worker dimorphism relies on the balance between the development of a molecular queen phenotype in all insects and colony-scale inhibition of this phenotype via asymmetric interactions. This allows Polistes to be stable against intrinsic perturbations of molecular states while reacting plastically to extrinsic cues affecting the whole society. Long-term stability of the social structure is reinforced by dynamic DNA methylation. Our study provides a general principle of how both specialization and plasticity can be achieved in biological systems. A record of this paper's transparent peer review process is included in the supplemental information.

The aculeate wasps are one of the most diverse and speciose insect taxa; they are omnipresent across ecosystems and exhibit diverse co-evolutionary and exploitative associations with other organisms. There is widespread conjecture that aculeate wasps are likely to perform essential ecological and economic services of importance to the health, well-being and nutritional needs of our planet. However, the scope and nature of the ecosystem services they provide are not well understood relative to other insect groups (e.g. bees, butterflies, beetles), and appreciation of their value is further tarnished by their public reputation as pointless pests. Here, we conduct the first comprehensive review of how aculeate wasps contribute to the four main areas of ecosystem services: regulatory, provisioning, supporting and cultural services. Uniting data from a large but previously disconnected literature on solitary and social aculeate wasps, we provide a synthesis on how these insects perform important ecosystem services as parasitoids, predators, biological indicators, pollinators, decomposers and seed dispersers; and their additional services as a sustainable alternative to meat for human consumption, and medicinal potential as sources of research leads for anti-microbials and cancer treatments. We highlight how aculeate wasps offer substantial, but largely overlooked, economic benefits through their roles in natural pest management and biological control programs. Accordingly, we provide data-driven arguments for reasons to consider the ecosystem service value of aculeate wasps on a par with other ‘useful’ insects (e.g. bees). Finally, we provide a research roadmap identifying the key areas of research required to capitalise better on the services provided by these important insects.

1. Ecological citizen science initiatives are growing in popularity with the increasing realisation of the potential for occurrence records to contribute information on biodiversity. However, citizen science data are justifiably criticised for misidentification, uneven sampling, incomplete detection or selective reporting. 2. Here, we test the accuracy of citizen science data for UK social wasp (Vespinae) species’ distributions. We compared data collected over two weeks by members of the public setting out baited traps across the UK and sending captured specimens for expert identification (1294 locations; 6680 wasps; 3 dominant species Vespula vulgaris (44%), V. germanica (44%), and Vespa crabro (6%)), with a four-decade long-term dataset established by the Bees, Wasps and Ants Recording Society (BWARS). 3. The citizen science data were significantly less spatially biased than the long-term data, but they were more urban-biased. Species distribution modelling showed that, for Vespa crabro, just two weeks of citizen science generated coverage comparable to more than four decades of expert recording. 4. Overall, we show that citizen science can be an extremely powerful and robust method for mapping insect diversity and distributions. We suggest that cautious combination of citizen science data with long-term expert surveying could be a highly reliable method for monitoring biodiversity.

Stable social groups usually consist of families. However, recent studies have revealed higher level social structure, with interactions between family groups across different levels of social organization in multiple species. The explanations for why this apparently paradoxical behaviour arises appear to be varied and remain untested. Here, we use automated radio-tagging data from over 1000 wasps from 93 nests and social network analyses of over 30 000 nest visitation records to describe and explain interactions across levels of social organization in the eusocial paper wasp Polistes canadensis . We detected three levels of social organization (nest, aggregation and community) which exchange ‘drifter’ individuals within and between levels. The highest level (community) may be influenced by the patchiness of high-quality nesting habitats in which these insects exist. Networks of drifter movements were explained by the distance between nests, the group size of donor nests and the worker-to-brood ratios on donor and recipient nests. These findings provide some explanation for the multi-level social interactions, which may otherwise seem paradoxical. Fitness benefits across multiple levels of social organization should be considered when trying to understand animal societies.

1. The current dearth of long‐term insect population trends is a major obstacle to conservation. Occupancy models have been proposed as a solution, but it remains unclear whether they can yield long‐term trends from natural history collections, since specimen records are normally very sparse. A common approach for sparse data is to coarsen its spatial and/or temporal resolution, although coarsening risks violating model assumptions. 2. We (i) test whether occupancy trends of three social wasp (Hymenoptera: Vespidae: Vespinae) species – the common wasp (Vespula vulgaris), the German wasp (Vespula germanica) and the European hornet (Vespa crabro) – have changed in England between 1900 and 2016, and (ii) test the effect of spatiotemporal resolution on the performance of occupancy models using very sparse data. All models are based on an integrated dataset of occurrence records and natural history collection specimen records. 3. We show that occupancy models can yield long‐term species‐specific trends from very sparse natural history collection specimens. We present the first quantitative trends for three Vespinae species in England over 116 years. Vespula vulgaris and V. germanica show stable trends over the time series, whilst V. crabro's occupancy decreased from 1950 to 1970 and increased since 1970. Moreover, we show that spatiotemporal resolution has little effect on model performance, although coarsening the spatial grain is an appropriate method for achieving enough records to estimate long‐term changes. 4. With the increasing availability of biological records, the model formulation used here has the potential to provide novel insights by making use of natural history collections' unique specimen assemblages.

Phenotypic plasticity provides organisms with the potential to adapt to their environment and can drive evolutionary innovations. Developmental plasticity is environmentally induced variation in phenotypes during development that arise from a shared genomic background. Social insects are useful models for studying the mechanisms of developmental plasticity, due to the phenotypic diversity they display in the form of castes. However, the literature has been biased toward the study of developmental plasticity in the holometabolous social insects (i.e., bees, wasps, and ants); the hemimetabolous social insects (i.e., the termites) have received less attention. Here, we review the phenotypic complexity and diversity of termites as models for studying developmental plasticity. We argue that the current terminology used to define plastic phenotypes in social insects does not capture the diversity and complexity of these hemimetabolous social insects. We suggest that terminology used to describe levels of cellular potency could be helpful in describing the many levels of phenotypic plasticity in termites. Accordingly, we propose a conceptual framework for categorizing the changes in potential of individuals to express alternative phenotypes through the developmental life stages of termites. We compile from the literature an exemplar dataset on the phenotypic potencies expressed within and between species across the phylogeny of the termites and use this to illustrate how the potencies of different life stages of different species can be described using this framework. We highlight how this conceptual framework can help exploit the rich phenotypic diversity of termites to address fundamental questions about the evolution and mechanisms of developmental plasticity. This conceptual contribution is likely to have wider relevance to the study of other hemimetabolous insects, such as aphids and gall-forming thrips, and may even prove useful for some holometabolous social insects which have high caste polyphenism.

Major evolutionary transitions describe how biological complexity arises; e.g. in evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. Castes across different evolutionary lineages are thought to be regulated by a conserved genetic toolkit. However, this hypothesis has not been tested thoroughly across the complexity spectrum of the major transition. Here we reveal, using machine learning analyses of brain transcription, evidence of a shared genetic toolkit across the spectrum of social complexity in Vespid wasps. Whilst molecular processes underpinning the simpler societies (which likely represent the origins of social living) are conserved throughout the major transition, additional processes appear to come into play in more complex societies. Such fundamental shifts in regulatory processes with complexity may typify other major evolutionary transitions, such as the evolution of multicellularity.

Phenotypic plasticity, the ability to produce multiple phenotypes from a single genotype, represents an excellent model with which to examine the relationship between gene expression and phenotypes. Despite this, analyses of the molecular bases of plasticity have been limited by the challenges of linking individual phenotypes with individual-level gene expression profiles, especially in the case of complex social phenotypes. Here, we tackle this challenge by analysing the individual-level gene expression profiles of Polistes dominula paper wasps following the loss of a queen, a perturbation that induces some individuals to undergo a significant phenotypic shift and become replacement reproductives. Using a machine learning approach, we find a strong response of caste-associated gene expression to queen loss, wherein individuals’ expression profiles become intermediate between queen and worker states. Importantly, this change occurs even in individuals that appear phenotypically unaffected. Part of this response is explained by individual attributes, most prominently age. These results demonstrate that large changes in gene expression may occur in the absence of detectable phenotypic changes, resulting here in a socially mediated de-differentiation of individuals at the transcriptomic but not the phenotypic level. Our findings also highlight the complexity of the relationship between gene expression and phenotype, where transcriptomes are neither a direct reflection of the genotype nor a proxy for the molecular underpinnings of the external phenotype.

Phenotypic plasticity, the ability to produce multiple phenotypes from a single genotype, represents an excellent model with which to examine the relationship between gene expression and phenotypes. Despite this, analyses of the molecular bases of plasticity have been limited by the challenges of linking individual phenotypes with individual-level gene expression profiles, especially in the case of complex social phenotypes. Here, we tackle this challenge by analysing the individual-level gene expression profiles of Polistes dominula paper wasps following the loss of a queen, a perturbation that induces some individuals to undergo a significant phenotypic shift and become replacement reproductives. Using a machine learning approach, we find a strong response of caste-associated gene expression to queen loss, wherein individuals’ expression profiles become intermediate between queen and worker states. Importantly, this change occurs even in individuals that appear phenotypically unaffected. Part of this response is explained by individual attributes, most prominently age. These results demonstrate that large changes in gene expression may occur in the absence of detectable phenotypic changes, resulting here in a socially mediated de-differentiation of individuals at the transcriptomic but not the phenotypic level. Our findings also highlight the complexity of the relationship between gene expression and phenotype, where transcriptomes are neither a direct reflection of the genotype nor a proxy for the molecular underpinnings of the external phenotype.

Altruism between close relatives can be easily explained. However, paradoxes arise when organisms divert altruism towards more distantly related recipients. In some social insects, workers drift extensively between colonies and help raise less related foreign brood, seemingly reducing inclusive fitness. Since being highlighted by W. D. Hamilton, three hypotheses (bet hedging, indirect reciprocity and diminishing returns to cooperation) have been proposed for this surprising behaviour. Here, using inclusive fitness theory, we show that bet hedging and indirect reciprocity could only drive cooperative drifting under improbable conditions. However, diminishing returns to cooperation create a simple context in which sharing workers is adaptive. Using a longitudinal dataset comprising over a quarter of a million nest cell observations, we quantify cooperative payoffs in the Neotropical wasp Polistes canadensis, for which drifting occurs at high levels. As the worker-to-brood ratio rises in a worker’s home colony, the predicted marginal benefit of a worker for expected colony productivity diminishes. Helping related colonies can allow effort to be focused on related brood that are more in need of care. Finally, we use simulations to show that cooperative drifting evolves under diminishing returns when dispersal is local, allowing altruists to focus their efforts on related recipients. Our results indicate the power of nonlinear fitness effects to shape social organization, and suggest that models of eusocial evolution should be extended to include neglected social interactions within colony networks. Altruism towards distantly related recipients appears to reduce inclusive fitness and is difficult to understand. Here, the authors quantify cooperative payoffs in a Neotropical wasp with high levels of movement between colonies and use inclusive fitness theory to show that diminishing returns to cooperation explain this behaviour.

Transmission of honey bee viruses to other insects, and vice versa, has previously been reported and the true ecological importance of this phenomenon is still being realized. Members of the family Vespidae interact with honey bees via predation or through the robbing of brood or honey from colonies, and these activities could result in virus transfer. In this study we screened Vespa velutina and Vespa crabro collected from Europe and China and also honey bees and Vespula vulgaris from the UK for Moku virus (MV), an Iflavirus first discovered in the predatory social wasp Vespula pensylvanica in Hawaii. MV was found in 71% of Vespula vulgaris screened and was also detected in UK Vespa crabro. Only seven percent of Vespa velutina individuals screened were MV-positive and these were exclusively samples from Jersey. Of 69 honey bee colonies screened, 43% tested positive for MV. MV replication was confirmed in Apis mellifera and Vespidae species, being most frequently detected in Vespula vulgaris. MV sequences from the UK were most similar to MV from Vespula pensylvanica compared to MV from Vespa velutina in Belgium. The implications of the transfer of viruses between the Vespidae and honey bees are discussed.

Sex-biased dispersal is common in social species, but the dispersing sex may delay emigration if associated benefits are not immediately attainable. In the social Hymenoptera (ants, some bees and wasps), newly emerged males typically disperse from the natal nest whilst most females remain as philopatric helpers. However, little information exists on the mechanisms regulating male dispersal. Furthermore, the conservation of such mechanisms across the Hymenoptera and any role of sexual maturation are also relatively unknown. Through field observations and mark-recapture, we observed that males of the social paper wasp

Biological systems not only have the remarkable capacity to build and maintain complex spatio-temporal structures in noisy environments, they can also rapidly break up and rebuild such structures. How such systems can simultaneously achieve both robust specialisation and plasticity is poorly understood. Here we use primitive societies ofPolisteswasps as a model system where we experimentally perturb the social structure by removing the queen and follow the re-establishment of the social steady state over time. We combine a unique experimental strategy correlating time-resolved measurements across vastly different scales with a theoretical approach. We show thatPolistesintegrates antagonistic processes on multiple scales to distinguish between extrinsic and intrinsic perturbations and thereby achieve both robust specialisation and rapid plasticity. The long-term stability of the social structure relies on dynamic DNA methylation which controls transcriptional noise. Such dynamics provide a general principle of how both specialization and plasticity can be achieved in biological systems.One Sentence SummaryA primitive social insect simultaneously achieves specialisation and plasticity by integrating antagonistic dynamics on different scales.HighlightsWe employ a unique experimental approach correlating dynamics of societies, individuals, and epigenetic gene regulationA social insect simultaneously achieves specialisation and plasticity by integrating antagonistic processes on different spatial scalesRegulation of population-level noise by DNA methylation ensures long-term stability of phenotypic specialisation

1. The potential decline of insects and their contribution to ecosystem services is a matter of immense concern. 2. Reversing the current degradation of the natural world will require substantial attitudinal and behavioural shifts, but for this to occur people will need to buy‐in to decisions and choices that may be less desirable than those they currently make. 3. People will also need to appreciate the importance of ecosystems, habitats and species that are currently regarded as uncharismatic, including of course a great many insects and other invertebrates. To do this requires a radical shift in our approach to marketing the natural world in general and insects in particular. 4. We propose adopting the approach used so successfully in commercial marketing; the 4Ps framework (product, price, place and promotion). We outline examples of how this would result in more informed and effective ways to market biodiversity, expanding focus away from species traditionally considered charismatic. The public perception of insects, a group that includes some of the most loved and many of the most disliked taxa on the planet, could potentially be substantially improved by the use of this approach. 5. If such a marketing strategy can raise their perceived value, it follows that the public may care more about insects and empower conservation action.

The strong coevolutionary arms race between social parasites and their hosts has dramatically shaped the life-history traits of both parties. One of the main strategies exhibited by hosts in response to parasitism is reproduction by host workers. We lack a mechanistic understanding of how these defence strategies unfold and, specifically, whether hosts exhibit more subtle strategies to reduce the costs of parasitism from the outset. Here we test the hypothesis that there are both behavioural and neurogenomic signatures of worker responses to parasitism, prior to overt expression in the form of egg-laying; we test this using the social parasite—social host system of the paper wasps Polistes sulcifer-Polistes dominula. We characterized individual workers’ position within the social interaction network of queenright and host colonies immediately after parasite usurpation, weeks before the workers’ reproductive rebellion is evident. Parasitism influenced network centrality measures, with workers in parasitized colonies showing increased connectedness and centrality compared to those in unparasitized ones. Next, we quantified brain gene expression levels for five genes related to physiological and behavioural phenotypes in Polistes wasps. The gene Imaginal disc growth factor (Idgf4), thought to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies; this may be an indication that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion. Our results provide the first evidence of early behavioural and neurogenomic responses of host workers toward the presence of an inquiline social parasite in a social insect.

All the supplementary information for the article is here.

Reproduction in cooperative animal groups is often dominated by one or a few individuals, with the remaining group members relegated to nonreproductive helping roles. This reproductive skew can evolve if helpers receive fitness benefits such as potential future inheritance of the breeding position, but the mechanisms by which inheritance is determined are not well resolved. Polistes paper wasps form highly reproductively skewed groups and inheritance of the breeding position is likely to play a key role in the maintenance of this social structure, making them excellent models for the processes by which simple societies are maintained. Reproductive succession is thought to be determined via an age-based convention in some Polistes species, but there is also evidence for contest-based succession systems in which the replacement queen uses physical aggression to overpower and thereby subordinate her nestmates. Here, we provide evidence that queen succession in colonies of the European paper wasp Polistes dominula is determined via convention rather than contest, with little disruption to the colony’s social functioning. We use queen removal experiments and fine-scale behavioral analyses to confirm that age is a strong predictor of succession, and that behavioral responses to queen removal are restricted to the oldest individuals rather than being experienced equally across the group. We provide the most comprehensive and detailed experimental analysis on the dynamics of breeder succession in a cooperatively breeding invertebrate to date, thereby shedding light on the mechanisms by which animal societies are able to maintain cohesion in the face of within-group conflict.

The evolution of altruism—costly self-sacrifice in the service of others—has puzzled biologists1 since The Origin of Species. For half a century, attempts to understand altruism have developed around the concept that altruists may help relatives to have extra offspring in order to spread shared genes2. This theory—known as inclusive fitness—is founded on a simple inequality termed Hamilton’s rule2. However, explanations of altruism have typically not considered the stochasticity of natural environments, which will not necessarily favour genotypes that produce the greatest average reproductive success,3,4. Moreover, empirical data across many taxa reveal associations between altruism and environmental stochasticity,5–8, a pattern not predicted by standard interpretations of Hamilton’s rule. Here we derive Hamilton’s rule with explicit stochasticity, leading to new predictions about the evolution of altruism. We show that altruists can increase the long-term success of their genotype by reducing the temporal variability in the number of offspring produced by their relatives. Consequently, costly altruism can evolve even if it has a net negative effect on the average reproductive success of related recipients. The selective pressure on volatility-suppressing altruism is proportional to the coefficient of variation in population fitness, and is therefore diminished by its own success. Our results formalize the hitherto elusive link between bet-hedging and altruism4,9–11, and reveal missing fitness effects in the evolution of animal societies.

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.

Explaining the evolution of helping behaviour in the eusocial insects where non-reproductive ('worker') individuals help raise the offspring of other individuals ('queens'), remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on non-tropical species, where seasonality causes family groups to disperse; cofoundresses forming new colonies the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes - Polistes canadensis. Using both microsatellites and newly-developed single-nucleotide polymorphism (SNP) markers we show that adult cofoundresses are highly related, and that brood production is monopolised by a single female across the nesting cycle. Non-reproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life-history and ecologies when considering the evolution of reproductive strategies.

Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome-wide transcriptional profiling using RNA-Sequencing (RNA-Seq) of S. bombi-infected Bombus terrestris queens at two critical time-points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signalling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host-parasite interaction.

The reversal of the fecundity/longevity tradeoff in social insects is striking, but we lack understanding of when and how this reversal evolved. Vespid wasps are excellent models for studying social evolution because species show different levels of sociality from solitary to primitively to advanced eusocial. We provide the first synthesis of existing, but scanty, data available on longevity in vespids. We explore whether the fecundity/longevity tradeoff reversal is exaggerated in species with more derived sociality. Although the reversal is evident in primitively social wasps, the available data suggest it may be stronger in large-colonied species, which show a trend toward shorter worker longevity. More data are needed on additional species and underlying mechanisms, but vespids hold promise for understanding the evolution of the fecundity/longevity tradeoff reversal.

Insect pollinators such as bumblebees (Bombus spp.) are in global decline1,2, a major cause of which is habitat loss due to agricultural intensification3. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed4-6. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages7, in target species. Such understanding is lacking for bumblebees because of the difficulty of systematically finding and monitoring colonies in the wild. We used a novel combination of habitat manipulation, land-use and habitat surveys, molecular genetics8 and demographic and spatial modelling to examine between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250-1000 m of the natal colony. This is the first evidence of a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. The findings provide strong support for conservation interventions that increase floral resources at a landscape scale and throughout the season having positive effects on wild pollinators in agricultural landscapes.

Conspecific acceptance thresholds (Reeve 1989 Am. Nat. 133 , 407–435), which have been widely applied to explain ecological behaviour in animals, proposed how sensory information, prior information and the costs of decisions determine actions. Signal detection theory (Green & Swets 1966 Signal detection theory and psychophysics ; SDT), which forms the basis of CAT models, has been widely used in psychological studies to partition the ability to discriminate sensory information from the action made as a result of it. In this article, we will review the application of SDT in interpreting the behaviour of laboratory animals trained in operant conditioning tasks and then consider its potential in ecological studies of animal behaviour in natural environments. Focusing on the nest-mate recognition systems exhibited by social insects, we show how the quantitative application of SDT has the potential to transform acceptance rate data into independent indices of cue sensitivity and decision criterion (also known as the acceptance threshold). However, further tests of the assumptions underlying SDT analysis are required. Overall, we argue that SDT, as conventionally applied in psychological studies, may provide clearer insights into the mechanistic basis of decision making and information processing in behavioural ecology. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Major evolutionary transitions in individuality are characterised by the formation of new levels of biological complexity from the cooperation of previously independent lower-level units. The evolution of superorganismality in insects is one such major transition, and is characterised by an extreme division of reproductive labour between ancestrally autonomous units, in the form of queen and worker castes. Here, we discuss the nature of plasticity in the emergence of castes across the major transition to superorganismality in insects. We identify key changes in plasticity which act at different levels of selection: a loss of reproductivity plasticity at the individual level is matched by a gain in plasticity at the colony level. Taking multi-level selection into consideration has important implications for formulating testable hypotheses regarding the nature of plasticity in a major transition from a lower to a higher level of biological complexity.

Seed dispersal is a fundamental process in the lifecycle of all flowering plants. Many plant species have evolved specialist associations with biotic vectors to facilitate dispersal. Such specialised interactions mean that these associations are potentially highly sensitive to disruption, e.g. from invasive species. However, despite this threat we still understand remarkably little about how such perturbations affect the dynamics and efficiency of the seed-dispersal process. In this study we quantify the impacts of an invasive ant across three key phases of the seed dispersal process: seed removal, distribution and placement, in order to determine the stages of seed dispersal most vulnerable to disruption by invaders. Using the Argentine ant (Linepithema humile) as a model, we show that invaded sites exhibited a significant decrease in seed dispersal services across all three phases of the dispersal process, relative to non-invaded sites. Seeds dispersed in invaded sites were: (a) less likely to be transported; (b) potentially distributed over a smaller spatial area, and (c) less likely to be placed at soil depths favourable for germination and establishment compared to those dispersed in non-invaded sites. These results reveal that ant-mediated seed dispersal services are significantly reduced by an invasive species at multiple stages in the dispersal process. Reductions in the efficacy of seed dispersal, combined with shifts in the ecological and geographical patterns of dispersal, may lead to cascading impacts on plant species composition and community structure. This study shows how an invasive ant can affect seed dispersal at several stages in the dispersal process This work was funded by grants from the COST Action TD1209 (ECOSTSTSM-TD1209: 070915-062123, 010715-062122, and 160614-046307) and a National Environmental Research Council Case Studentship awarded to SS, JB and RN (NE/K007076/1)

The major evolutionary transition to superorganismality has taken place several times in the insects. Although there has been much consideration of the ultimate evolutionary explanations for superorganismality, we know relatively little about what proximate mechanisms constrain or promote this major transition. Here, we propose that Vespid wasps represent an understudied, but potentially very useful, model system for studying the mechanisms underpinning superorganismality. We highlight how there is an abundance of behavioural data for many wasp species, confirming their utility in studies of social evolution; however, there is a sparsity of genomic data from which we can test proximate and ultimate hypotheses on this major evolutionary transition.