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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’.

Extreme weather events, like high temperatures and droughts, are predicted to become common with climate change, and may negatively impact plant growth. How honey bees (Apis mellifera L. [Hymenoptera: Apidae]) will respond to this challenge is unclear, especially when collecting pollen, their primary source of protein, lipids, and micro-nutrients. We explored this response with a data set from multiple research projects that measured pollen collected by honey bees during 2015–2017 in which above-average temperatures and a drought occurred in 2017. We summarized the abundance and diversity of pollen collected from July to September in replicated apiaries kept at commercial soybean and corn farms in Iowa, in the Midwestern USA. The most commonly collected pollen was from clover (Trifolium spp. [Fabales: Fabaceae]), which dramatically declined in absolute and relative abundance in July 2017 during a period of high temperatures and drought. Due to an apparent lack of clover, honey bees switched to the more drought-tolerant native species (e.g., Chamaecrista fasciculata [Michx.] Greene [Fabales: Fabaceae], Dalea purpurea Vent. [Fabales: Fabaceae], Solidago spp. [Asterales: Asteraceae]), and several species of Asteraceae. This was especially noticeable in August 2017 when C. fasciculata dominated (87%) and clover disappeared from bee-collected pollen. We discuss the potential implications of climate-induced forage dearth on honey bee nutritional health. We also compare these results to a growing body of literature on the use of native, perennial flowering plants found in Midwestern prairies for the conservation of beneficial insects. We discuss the potential for drought resistant-native plants to potentially promote resilience to climate change for the non-native, managed honey bee colonies in the United States.

Ecosystems are interconnected and complex, but conservation has often focused on rehabilitating individual species. A systems-ecology approach aims to support overall structure and maintain functions of the whole ecosystem, and may be especially pertinent for mutualistic plant-pollinator communities. This approach focuses on species interactions as the units to be conserved within the larger ecosystem. Analyzing species interactions is a more holistic approach because it incorporates a broader web of organisms, and considers the plethora of potential indirect influences from interacting partners. In this article, we suggest pollinator researchers focus on plant-pollinator networks to inform conservation programs and best support the coexistence of pollinators and plants within natural and agricultural systems. We propose that a system-ecology perspective is the most promising way to simultaneously improve pollinator conservation, agricultural sustainability, and human well-being.

Hygienic behavior is a social defense mechanism against parasites and pathogens in honeybees. We studied the genetic basis of hygienic behavior in African-derived Apis mellifera by performing RNA sequencing on brains of individual honeybee workers observed performing hygienic behavior, in order to identify expression changes linked with this behavior. We also used the transcriptome data to search for single nucleotide polymorphism (SNP) variation in genes previously associated with the trait in other A. mellifera populations. The analysis revealed 49 differentially expressed genes (DEG), most of them upregulated during hygienic acts. One DEG, Apidaecin, also showed SNP variation across samples, providing a promising candidate gene for both expression-based and heritable variation in hygienic behavior. We also identified 27 additional SNPs in the coding regions of five candidate genes previously linked with honeybee hygienic behavior. These results provide a useful starting place to analyze the genetic basis of hygienic behavior in African-derived honeybees.

In 2006, the full complement of DNA sequence information (or ‘genome’) of the Western honey bee, Apis mellifera, was published. This important resource was one of the most important advances in the history of honey bee research, with seemingly limitless applications to unlocking the secrets of honey bee biology and social life and for improving health, breeding and management. Honey bee genomics has seen immense growth in the past one and a half decades. In this article, we reflect on what the genome has added to our understanding of fundamental aspects of honey bee biology, including evolutionary origins, behaviour and health/disease. We conclude that while the genome has fuelled growth in many areas of honey bee research, it is only one part of an emerging systems-based, multi-omics approach. Moving forward, we posit that honey bee research will benefit most from an even fuller integration of genomics with classical approaches in evolution, ethology, physiology and microbiology.

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.

Intensified agriculture reduces natural and seminatural habitats and plant diversity, reducing forage available to honey bees (Apis mellifera L. [Hymenoptera: Apidea]). In agricultural landscapes of Iowa, United States, we studied the impact of extrinsic agricultural intensification on the availability of pollen for honey bees by placing colonies next to soybean fields surrounded by either a low or high level of cultivation. The abundance and diversity of pollen returned to a colony were estimated by placing pollen traps on bee colonies during the summer and fall of 2015 and 2016. We observed no difference in abundance and diversity of pollen collected by colonies in either landscape, but abundance varied over time with significantly less collected in September. We explored if the most commonly collected pollen from these landscapes had the capacity to support honey bee immune health by testing if diets consisting of these pollens improved bee resistance to a viral infection. Compared to bees denied pollen, a mixture of pollen from the two most common plant taxa (Trifolium spp. L. [Fabales: Fabaceae] and Chimaechrista fasciculata (Michx.) Greene [Fabales: Fabaceae]) significantly reduced honey bee mortality induced by viral infection. These data suggest that a community of a few common plants was favored by honey bees, and when available, could be valuable for reducing mortality from a viral infection. Our data suggest a late season shortage of pollen may be ameliorated by additions of fall flowering plants, like goldenrod (Solidago spp. L. [Asterales: Asteraceae]) and sunflower (Helianthus, Heliopsis, and Silphium spp. [Asterales: Asteraceae]), as options for enhancing pollen availability and quality for honey bees in agricultural landscapes.

In the last century, a global transformation of Earth’s surface has occurred due to human activity with extensive agriculture replacing natural ecosystems. Concomitant declines in wild and managed bees are occurring, largely due to a lack of floral resources and inadequate nutrition, caused by conversion to monoculture-based farming. Diversified fruit and vegetable farms may provide an enhanced variety of resources through crops and weedy plants, which have potential to sustain human and bee nutrition. We hypothesized fruit and vegetable farms can enhance honey bee (Hymenoptera: Apidae, Apis mellifera Linnaeus) colony growth and nutritional state over a soybean monoculture, as well as support a more diverse wild bee community. We tracked honey bee colony growth, nutritional state, and wild bee abundance, richness, and diversity in both farm types. Honey bees kept at diversified farms had increased colony weight and preoverwintering nutritional state. Regardless of colony location, precipitous declines in colony weight occurred during autumn and thus colonies were not completely buffered from the stressors of living in a matrix dominated with monocultures. Contrary to our hypothesis, wild bee diversity was greater in soybean, specifically in August, a time when fields are in bloom. These differences were largely driven by four common bee species that performed well in soybean. Overall, these results suggest fruit and vegetable farms provide some benefits for honey bees; however, they do not benefit wild bee communities. Thus, incorporation of natural habitat, rather than diversified farming, in these landscapes, may be a better choice for wild bee conservation efforts.

Native pollinators are important for providing vital services in agroecosystems; however, their numbers are declining globally. Bees are the most efficient and diverse members of the pollinator community; therefore, it is imperative that management strategies be implemented that positively affect bee community composition and health. Here, we test responses of the bee and flowering plant communities to land management treatments in the context of grasslands in the upper Midwestern United States, a critical area with respect to bee declines. Twelve sites were selected to examine floral resources and wild bee communities based on three different types of grasslands: tallgrass prairie remnants, ungrazed restorations, and grazed restorations. Total bee abundance was significantly higher in ungrazed restorations than remnants, but there were no significant differences among grasslands in community composition or Shannon diversity. Across the three grassland types we also examined mass and lipid stores as nutritional health indicators in three sweat bees (Halictidae), Augochlora pura, Agapostemon virescens, and Halictus ligatus. Although there were no differences in lipid content, total average bee mass was significantly higher in Ag. virescens collected from ungrazed restorations as compared to remnants. Floral abundance of native and non-native species combined was significantly higher in grazed restorations compared to remnants and ungrazed restorations. However, ungrazed restorations had higher abundance and richness of native flowering ramets. These data suggest that bee abundance and nutrition are driven by high abundance of native flowering plant species, rather than total flowering plants.

The north central state of Iowa is heavily dominated by agriculture, with limited nesting and foraging habitat for wild and managed pollinators. This region has been identified as critical for pollinator conservation for bees and non-bee species (e.g., monarch butterfly [Danaus plexippus]). Pollinator sustainability (i.e., wild bee conservation and sustainable beekeeping) relies upon management decisions by beekeepers, farmers, and landowners, but it is unclear if these stakeholders are aware of and use best practices. We present results of surveys administered to Iowan beekeepers, farmers, and landowners after extension programming on best management practices for sustaining honey bees (Apis mellifera) and other pollinators. Results show beekeepers, farmers, and landowners believe implementing pollinator-friendly practices is important. However, knowledge of tools to implement these practices, such as registering apiaries to avoid pesticide drift or cost-share programs for establishing habitat on their land, was very low. These results suggest opportunities exist for connecting beekeepers seeking higher quality apiaries with landowners that have established habitat with added floral resources. Further, we reviewed practices that reconstruct tallgrass prairie with support of federal cost-share funds, specifically CP42 and CP43 of the USDA’s conservation reserve program. Overall, we document strong support and enthusiasm for pollinator-friendly practices in Iowa but note gaps in knowledge of practices that are most effective and what tools are available to implement them. These results suggest a way for pollinator extension programs to address these knowledge gaps in a receptive group of beekeepers, farmers, and landowners.

The consequences of early-life experiences are far reaching. In particular, the social and nutritional environments that developing animals experience can shape their adult phenotypes. In honeybees, larval nutrition determines the eventual social roles of adults as reproductive queens or sterile workers. However, little is known about the effects of developmental nutrition on important adult worker phenotypes such as disease resilience. In this study, we manipulated worker developmental nutrition in two distinct ways under semi-natural field conditions. In the first experiment, we restricted access to nutrition via social isolation by temporarily preventing alloparental care. In the second experiment, we altered the diet quality experienced by the entire colony, leading to adult bees that had developed entirely in a nutritionally restricted environment. When bees from these two experiments reached the adult stage, we challenged them with a common bee virus, Israeli acute paralysis virus (IAPV) and compared mortality, body condition, and the expression of immune genes across diet and viral inoculation treatments. Our findings show that both forms of early life nutritional stress, whether induced by lack of alloparental care or diet quality restriction, significantly reduced bees’ resilience to virus infection and affected the expression of several key genes related to immune function. These results extend our understanding of how early life nutritional environment can affect phenotypes relevant to health and highlight the importance of considering how nutritional stress can be profound even when filtered through a social group. These results also provide important insights into how nutritional stress can affect honeybee health on a longer time scale and its potential to interact with other forms of stress (i.e. disease).

Significance Industrial-scale production of crops through monocultures has resulted in “green deserts” of reduced biodiversity in many areas worldwide. Such simplified landscapes may impact ecosystem services such as pollination. Here, we present a large-scale, longitudinal study of managed honey bee colonies in the context of corn and soybean monocultures. Our results reveal a brief burst of colony growth during soybean bloom, followed by a longer period of forage dearth, resulting in decline in several aspects of honey bee health at both colony and individual levels. We demonstrate this decline is reversible when honey bees have access to native, perennial plants (i.e., prairie). Our results suggest sustainable pollinator management in landscapes dominated by monocultures can be achieved through reintegration of native biodiversity., Intensive agriculture can contribute to pollinator decline, exemplified by alarmingly high annual losses of honey bee colonies in regions dominated by annual crops (e.g., midwestern United States). As more natural or seminatural landscapes are transformed into monocultures, there is growing concern over current and future impacts on pollinators. To forecast how landscape simplification can affect bees, we conducted a replicated, longitudinal assessment of honey bee colony growth and nutritional health in an intensively farmed region where much of the landscape is devoted to production of corn and soybeans. Surprisingly, colonies adjacent to soybean fields surrounded by more cultivated land grew more during midseason than those in areas of lower cultivation. Regardless of the landscape surrounding the colonies, all experienced a precipitous decline in colony weight beginning in August and ended the season with reduced fat stores in individual bees, both predictors of colony overwintering failure. Patterns of forage availability and colony nutritional state suggest that late-season declines were caused by food scarcity during a period of extremely limited forage. To test if habitat enhancements could ameliorate this response, we performed a separate experiment in which colonies provided access to native perennials (i.e., prairie) were rescued from both weight loss and reduced fat stores, suggesting the rapid decline observed in these agricultural landscapes is not inevitable. Overall, these results show that intensively farmed areas can provide a short-term feast that cannot sustain the long-term nutritional health of colonies; reintegration of biodiversity into such landscapes may provide relief from nutritional stress.

Simple Summary Honey bees rely on pollen and nectar to provide nutrients to support their yearly colony cycle. Specifics of the cycle differ among geographic regions as do the species of flowering plants and the nutrients they provide. We examined responses of honey bees from two different queen lines fed pollens from locations that differed in floral species composition and yearly colony cycles. We detected differences between the queen lines in the amount of pollen they consumed and the size of their hypopharyngeal glands (HPG). There were also seasonal differences between the nutrient composition of pollens. Spring pollens collected from colonies in both locations had higher amino and fatty acid concentrations than fall pollens. There also were seasonal differences in responses to the pollens consumed by bees from both queen lines. Bees consumed more spring than fall pollen, but digested less of it so that bees consumed more protein from fall pollens. Though protein consumption was higher with fall pollen, HPG were larger in spring bees. Abstract Honey bee colonies have a yearly cycle that is supported nutritionally by the seasonal progression of flowering plants. In the spring, colonies grow by rearing brood, but in the fall, brood rearing declines in preparation for overwintering. Depending on where colonies are located, the yearly cycle can differ especially in overwintering activities. In temperate climates of Europe and North America, colonies reduce or end brood rearing in the fall while in warmer climates bees can rear brood and forage throughout the year. To test the hypothesis that nutrients available in seasonal pollens and honey bee responses to them can differ we analyzed pollen in the spring and fall collected by colonies in environments where brood rearing either stops in the fall (Iowa) or continues through the winter (Arizona). We fed both types of pollen to worker offspring of queens that emerged and open mated in each type of environment. We measured physiological responses to test if they differed depending on the location and season when the pollen was collected and the queen line of the workers that consumed it. Specifically, we measured pollen and protein consumption, gene expression levels (hex 70, hex 110, and vg) and hypopharyngeal gland (HPG) development. We found differences in macronutrient content and amino and fatty acids between spring and fall pollens from the same location and differences in nutrient content between locations during the same season. We also detected queen type and seasonal effects in HPG size and differences in gene expression between bees consuming spring vs. fall pollen with larger HPG and higher gene expression levels in those consuming spring pollen. The effects might have emerged from the seasonal differences in nutritional content of the pollens and genetic factors associated with the queen lines we used.

While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change., Shell et al. compare the molecular evolution of bee genomes across species with varying social behaviours. Their findings indicate that eusocial lineages tend to have more gene family expansion than weakly social lineages. Transcriptomic data suggests that social phenotype is a consistent driver of macroevolutionary genomic change.

Populations of wild and managed pollinators are declining in North America, and causes include increases in disease pressure and decreases in flowering resources. Tallgrass prairies can provide floral resources for managed honey bees (Hymenoptera: Apidae, Apis mellifera Linnaeus) and wild bees. Honey bees kept near prairies may compete with wild bees for floral resources, and potentially transfer viral pathogens to wild bees. Measurements of these potential interactions are lacking, especially in the context of native habitat conservation. To address this, we assessed abundance and richness of wild bees in prairies with and without honey bee hives present, and the potential spillover of several honey bee viruses to bumble bees (Hymenoptera: Apidae, Bombus Latrielle). We found no indication that the presence of honey bee hives over 2 yr had a negative effect on population size of wild bee taxa, though a potential longer-term effect remains unknown. All levels of viruses quantified in bumble bees were lower than those observed in honey bees. Higher levels of deformed wing virus and Israeli acute paralysis virus were found in Bombus griseocollis DeGeer (Hymenoptera: Apidae) collected at sites with hives than those without hives. These data suggest that the presence of honey bees in tallgrass prairie could increase wild bee exposure to viruses. Additional studies on cross-species transmission of viruses are needed to inform decisions regarding the cohabitation of managed bees within habitat utilized by wild bees.

To study how honey bees utilize forage resources and guide pollination management plans in crops, a multitude of methods have been developed, but most are time consuming, costly, and require specialized skills. Colored pan traps for monitoring activity-density are a simple, efficient, and cost-effective alternative, however, their usefulness for studying honey bees is not well described. We examined if trap color, location within a field, and the presence of managed colonies affected estimates of honey bee activity-density within soybean fields. Soybeans are visited by pollinators but do not require these visits for seed development. Pan traps, especially those colored blue, captured more honey bees when colonies were present. There were no differences in activity-density based on placement of traps within a field nor with increasing distance from colonies. Throughout the season, activity-density in soybeans was constant but tripled after soybean ceased blooming, suggesting spikes in pan trap captures may indicate periods of forage scarcity. Activity-density did not correlate with the population size of worker bees at a site, but did correlate with number of colonies present. We conclude that pan traps can be useful for assessing honey bee activity, particularly for estimating colony presence and identifying times of forage scarcity.

Identifying the genetic basis of behavior has remained a challenge for biologists. A major obstacle to this goal is the difficulty of examining gene function in an ecologically relevant context. New tools such as CRISPR/Cas9, which alter the germline of an organism, have taken center stage in functional genomics in non-model organisms. However, germline modifications of this nature cannot be ethically implemented in the wild as a part of field experiments. This impediment is more than technical. Gene function is intimately tied to the environment in which the gene is expressed, especially for behavior. Most lab-based studies fail to recapitulate an organism's ecological niche, thus most published functional genomics studies of gene-behavior relationships may provide an incomplete or even inaccurate assessment of gene function. In this review, we highlight RNA interference as an especially effective experimental method to deepen our understanding of the interplay between genes, behavior, and the environment. We highlight the utility of RNAi for researchers investigating behavioral genetics, noting unique attributes of RNAi including transience of effect and the feasibility of releasing treated animals into the wild, that make it especially useful for studying the function of behavior-related genes. Furthermore, we provide guidelines for planning and executing an RNAi experiment to study behavior, including challenges to consider. We urge behavioral ecologists and functional genomicists to adopt a more fully integrated approach which we call "ethological genomics". We advocate this approach, utilizing tools such as RNAi, to study gene-behavior relationships in their natural context, arguing that such studies can provide a deeper understanding of how genes can influence behavior, as well as ecological aspects beyond the organism that houses them.

Animal nutritional state can profoundly affect behaviour, including an individual's tendency to cooperate with others. We investigated how nutritional restriction at different life stages affects cooperative behaviour in a highly social species, Apis mellifera honeybees. We found that nutritional restriction affects a worker's queen pheromone response, a behavioural indicator of investment in group vs. individual reproduction. Nutritional restriction at the larval stage led to reduced ovary size and increased queen pheromone response, whereas nutritional restriction at the adult stage led to reduced lipid stores and reduced queen pheromone response. We argue that these differences depend upon the extent of reproductive plasticity at these life stages and that individual worker honeybees may adjust their behavioural and physiological traits in response to nutritional stress to invest nutritional resources in either their own or their colony's reproduction. These results support the role of nutritional stress in the maintenance of cooperative behaviour, and we suggest that historical nutritional scarcity may be an important contributor to the evolution of extreme forms of cooperation. A plain language summary is available for this article.

Despite a strong history of theoretical work on the mechanisms of social evolution, relatively little is known of the molecular genetic changes that accompany transitions from solitary to eusocial forms. Here, we provide the first genome of an incipiently social bee that shows both solitary and social colony organization in sympatry, the Australian carpenter bee Ceratina australensis. Through comparative analysis, we provide support for the role of conserved genes and cis-regulation of gene expression in the phenotypic plasticity observed in nest-sharing, a rudimentary form of sociality. Additionally, we find that these conserved genes are associated with caste differences in advanced eusocial species, suggesting these types of mechanisms could pave the molecular pathway from solitary to eusocial living. Genes associated with social nesting in this species show signatures of being deeply conserved, in contrast to previous studies in other bees showing novel and faster-evolving genes are associated with derived sociality. Our data provide support for the idea that the earliest social transitions are driven by changes in gene regulation of deeply conserved genes.

Declines in honey bee health have been attributed to multiple interacting environmental stressors; among the most important are forage/nutrition deficits and parasites and pathogens. Recent studies suggest poor honey bee nutrition can exacerbate the negative impacts of infectious viral and fungal diseases, and conversely, that common honey bee parasites and pathogens can adversely affect bee nutritional physiology. This sets up the potential for harmful feedbacks between poor nutrition and infectious disease that may contribute to spiraling declines in bee health. We suggest that improving bees' nutritional resilience should be a major goal in combating challenges to bee health; this approach can buffer bees from other environmental stressors such as pathogen infection.

Cooperation and aggression are ubiquitous in social groups, and the genetic mechanisms underlying these behaviours are of great interest for understanding how social group formation is regulated and how it evolves. In this study, we used a candidate gene approach to investigate the patterns of expression of key genes for cooperation and aggression in the brain of a primitively eusocial wasp, Polistes dominula, during colony founding, when multiple foundresses can join the same nest and establish subtle hierarchies of dominance. We used a comparative approach to select candidate genes for cooperation and aggression looking at two previously published studies on global gene expression in wasps and ants. We tested the expression of these genes in P. dominula wasps that were either displaying aggressive behaviour (dominant and single foundresses) or cooperation (subordinate foundresses and workers) towards nestmates. One gene in particular, the egg yolk protein vitellogenin, known for its reproductive role in insects, displayed patterns of expression that strongly matched wasp social rank. We characterize the genomic context of vitellogenin by building a head co-expression gene network for P. dominula, and we discuss a potential role for vitellogenin as a mediator of social interactions in wasps. Electronic supplementary material The online version of this article (10.1007/s00359-018-1252-6) contains supplementary material, which is available to authorized users.

Hymenoptera is the second-most sequenced arthropod order, with 52 publically archived genomes (71 with ants, reviewed elsewhere), however these genomes do not capture the breadth of this very diverse order (Figure 1, Table 1). These sequenced genomes represent only 15 of the 97 extant families. Although at least 55 other genomes are in progress in an additional 11 families (see Table 2), stinging wasps represent 35 (67%) of the available and 42 (76%) of the in progress genomes. A more comprehensive catalog of hymenopteran genomes is needed for research into the evolutionary processes underlying the expansive diversity in terms of ecology, behavior, and physiological traits within this group. Additional sequencing is needed to generate an assembly for even 0.05% of the estimated 1 million hymenopteran species, and we recommend premier level assemblies for at least 0.1% of the >150,000 named species dispersed across the order. Given the haplodiploid sex determination in Hymenoptera, haploid male sequencing will help minimize genome assembly issues to enable higher quality genome assemblies.

The specialized ability to learn and recall individuals based on distinct facial features is known in only a few, large-brained social taxa. Social paper wasps in the genus Polistes are the only insects known to possess this form of cognitive specialization. We analyzed genome-wide brain gene expression during facial and pattern training for two species of paper wasps (P. fuscatus, which has face recognition, and P. metricus, which does not) using RNA sequencing. We identified 237 transcripts associated with face specialization in P. fuscatus, including some transcripts involved in neuronal signaling (serotonin receptor and tachykinin). Polistes metricus that learned faces (without specialized learning) and P. fuscatus in social interactions with familiar partners (from a previous study) showed distinct sets of brain differentially expressed transcripts. These data suggest face specialization in P. fuscatus is related to shifts in the brain transcriptome associated with genes distinct from those related to general visual learning and social interactions.

Eusociality, a form of animal social organization involving sterile and reproductive castes, is a rare, but highly ecologically successful form of life. There are striking examples of eusocial species with populations that are ecologically dominant in their native ranges, as well as remarkably successful globally as invasive species; prominent examples include fire ants and yellowjacket wasps. At the same time, there have been startling population declines in other social insects, notably bumble bees. Here, we explore the possible role of phenotypic plasticity in invasion biology and declines of social insect species. This topic is of particular interest, because social insects exhibit extreme behavioral, developmental, physiological, and morphological plasticity. It has been suggested that this plasticity may contribute to ecological dominance in some species, but could be a liability or cost to others. In this review, we explore the relationship between phenotypic plasticity, invasion biology, and vulnerability to global change in social insects. By considering plasticity at three levels–molecular, individual, and colony—we suggest ways in which considerations of phenotypic plasticity may help in managing social insect populations. Fil: Manfredini, Fabio. University of London; Reino Unido. University of Aberdeen; Reino Unido Fil: Arbetman, Marina Paula. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; Argentina Fil: Toth, Amy L.. Iowa State University; Estados Unidos

Hormones are often major regulators of complex behaviors, such as mating and reproduction. In insects, juvenile hormone (JH) is integral to many components of reproductive physiology and behavior, but its role in female sexual receptivity is not well understood. To investigate the influence of JH on receptivity, we utilized the social wasp Polistes fuscatus. In Polistes, mating behavior is temporally separated from other components of reproduction, which allows for examination of the physiology and behavior of mating, disentangled from fertilization and egg-laying. We reared virgin gynes (reproductive females) in the lab and divided them into four groups, in which gynes received multiple topical treatments of either 20 μg, 10 μg, 5 μg, or 0 μg of the JH analog methoprene. Gynes were then placed in petri dishes with 2 unrelated males and we recorded attempted and successful mating. Additionally, we measured gyne ovarian development and survival in each group. We found that methoprene increased both sexual receptivity and ovarian development, but was associated with a decrease in long-term survival. Receptivity increased linearly as methoprene treatment increased, but the effect of methoprene on ovarian development was independent of dose. These results demonstrate the importance of JH in sexual receptivity and mating behavior. We argue that the relatively understudied Polistes gyne has potential as a model for mating and reproduction, and for the internal and external regulation of this complex behavior.

Although social behavior can have a strong genetic component, it can also result in selection on genome structure and function, thereby influencing the evolution of the genome itself. Here we explore the bidirectional links between social behavior and genome architecture by considering variation in social and/or mating behavior among populations (social polymorphisms) and across closely related species. We propose that social behavior can influence genome architecture via associated demographic changes due to social living. We establish guidelines to exploit emerging whole-genome sequences using analytical approaches that examine genome structure and function at different levels (regulatory vs structural variation) from the perspective of both molecular biology and population genetics in an ecological context.

Honeybee population declines have been linked to multiple stressors, including reduced diet diversity and increased exposure to understudied viral pathogens. Despite interest in these factors, few experimental studies have explored the interaction between diet diversity and viral infection in honeybees. Here, we used a mixture of laboratory cage and small semi-field nucleus hive experiments to determine how these factors interact. In laboratory experiments, we found that high-quality diets (polyfloral pollen and high-quality single-source pollen) have the potential to reduce mortality in the face of infection with Israeli acute paralysis virus (IAPV). There was a significant interaction between diet and virus infection on mortality, even in the presence of high virus titres, suggesting that good diets can help bees tolerate virus infection. Further, we found that extreme stress in the form of pollen starvation in conjunction with IAPV infection increase exiting behaviour from small experimental hives. Finally, we showed that higher-quality pollen diets have significantly higher iron and calcium content, suggesting micronutrient deficiencies could be an under-explored area of bee nutrition.

We develop a transdisciplinary deliberative model that moves beyond traditional scientific collaborations to include nonscientists in designing complexity-oriented research. We use the case of declining honey bee health as an exemplar of complex real-world problems requiring cross-disciplinary intervention. Honey bees are important pollinators of the fruits and vegetables we eat. In recent years, these insects have been dying at alarming rates. To prompt the reorientation of research toward the complex reality in which bees face multiple challenges, we came together as a group, including beekeepers, farmers, and scientists. Over a 2-year period, we deliberated about how to study the problem of honey bee deaths and conducted field experiments with bee colonies. We show trust and authority to be crucial factors shaping such collaborative research, and we offer a model for structuring collaboration that brings scientists and nonscientists together with the key objects and places of their shared concerns across time.

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.

Comparative genomics of social insects has been intensely pursued in recent years with the goal of providing insights into the evolution of social behaviour and its underlying genomic and epigenomic basis. However, the comparative approach has been hampered by a paucity of data on some of the most informative social forms (e.g. incipiently and primitively social) and taxa (especially members of the wasp family Vespidae) for studying social evolution. Here, we provide a draft genome of the primitively eusocial model insect Polistes dominula, accompanied by analysis of caste-related transcriptome and methylome sequence data for adult queens and workers. Polistes dominula possesses a fairly typical hymenopteran genome, but shows very low genomewide GC content and some evidence of reduced genome size. We found numerous caste-related differences in gene expression, with evidence that both conserved and novel genes are related to caste differences. Most strikingly, these -omics data reveal a major reduction in one of the major epigenetic mechanisms that has been previously suggested to be important for caste differences in social insects: DNA methylation. Along with a conspicuous loss of a key gene associated with environmentally responsive DNA methylation (the de novo DNA methyltransferase Dnmt3), these wasps have greatly reduced genomewide methylation to almost zero. In addition to providing a valuable resource for comparative analysis of social insect evolution, our integrative -omics data for this important behavioural and evolutionary model system call into question the general importance of DNA methylation in caste differences and evolution in social insects.

The existence of personalities has been explored in various invertebrates, but a comprehensive investigation of personality differences across individuals in a eusocial insect has not yet been conducted. The study of personality differences across individuals within the same behavioral caste may contribute to an understanding of how social insects divide labor within the nest. Here, we define and investigate three dimensions of personality within the worker caste of a model social insect, the honey bee Apis mellifera, as follows: (1) consistent individual behavioral differences over time, (2) consistent individual behavioral differences across contexts, and (3) the presence of correlated suites of behaviors. To test whether honey bee workers exhibit dimensions 1 and 2, we repeatedly assessed responses of groups of same-age bees in cages to stimuli that are relevant to bee life history. To test for dimension 3, we examined behavior within a colony context by using observation hives to record the behaviors of individual bees across their lifetimes. Our results provide some evidence for all three dimensions of personality in honey bee workers. In particular, our data suggest some individuals may be more likely to be highly interactive with other workers (e.g., engaging in food sharing), while other individuals are consistently less interactive. These findings expand upon and contribute to previous models for the organization of worker division of labor in honey bees, suggesting that consistent behavioral differences (personalities) of workers within a behavioral caste have the potential to contribute to subcaste division of labor. Behavioral ecologists have become increasingly interested in animal personalities, individual behavioral differences that are consistent over time and in different contexts, with recent focus on understanding the occurrence of personalities across taxa and their adaptive value. The existence and function of personality differences among individuals in complex societies, such as eusocial insects, remain understudied. Here, we provide the first comprehensive investigation of whether workers of the highly eusocial honey bee show hallmarks of personality. Although these workers demonstrate well-documented behavioral changes as they age, we uncovered some aspects of their behavior, in particular, their tendency to physically interact with other bees, remain somewhat consistent even as they age and change roles within the colony. We suggest that individual-level personality differences have the potential to contribute to colony division of labor by creating variation in individual tendencies to perform different tasks.

Grasslands provide important resources for pollinators in agricultural landscapes. Managing grasslands with fire and grazing has the potential to benefit plant and pollinator communities, though there is uncertainty about the ideal approach. We examined the relationships among burning and grazing regimes, plant communities, and Bombus species and Apis mellifera L. abundance and nutritional indicators at the Grand River Grasslands in southern Iowa and northern Missouri. Treatment regimes included burn-only, grazed-and-burned, and patch-burn graze (pastures subdivided into three temporally distinct fire patches with free access by cattle). The premise of the experimental design was that patch-burn grazing would increase habitat heterogeneity, thereby providing more diverse and abundant floral resources for pollinators. We predicted that both bee abundance and individual bee nutritional indicators (bee size and lipid content) would be positively correlated with floral resource abundance. There were no significant differences among treatments with respect to bee abundance. However, some of the specific characteristics of the plant community showed significant relationships with bee response variables. Pastures with greater abundance of floral resources had greater bee abundance but lower bee nutritional indicators. Bee nutritional variables were positively correlated with vegetation height, but, in some cases, negatively correlated with stocking rate. These results suggest grassland site characteristics such as floral resource abundance and stocking rate are of potential importance to bee pollinators and suggest avenues for further research to untangle the complex interactions between grassland management, plant responses, and bee health.

In social species, there is a fundamental trade-off between 'me' and 'we'; that is, should I reproduce, or should I work to help others to reproduce? In this issue of Molecular Ecology, Okada et al. () delve into the evolution and genetic mechanisms of this core question, focusing on social caste formation in insects. The authors take advantage of a unique ant in the genus Diacamma, which has secondarily lost the classic, highly different queens and workers found in many other ants, bees and wasps. Instead, Diacamma ant castes are decided via aggressive dominance interactions among adult females, similar to dominance hierarchies seen in primitively social insects and many social vertebrates. But how does being dominated translate into reproductive shutdown and thus, the creation of a worker caste? The authors use transcriptomics to address this question, and discover that the key may lie in very rapid (within one day) changes in the regulation of nutrient signalling genes, and other genes related to nutrient storage and reproduction. In other words, being aggressed turns on or off genes that tell the ant's brain and physiology to go into 'sterile mode', whereas winning a fight stimulates other genes that ramp up reproductive traits. These results add weight to the idea that caste differences rely on a 'toolkit' of deeply conserved genes involved in core nutritional, reproductive and metabolic functions. In addition, these results emphasize the exquisite and rapid social environmental sensitivity of core toolkit genes during the production of distinct phenotypes.

Eusociality has independently evolved multiple times in the hymenoptera, but the patterns of adaptive molecular evolution underlying the evolution and elaboration of eusociality remain uncertain. Here, we performed a population genomics study of primitively eusocial Polistes (paper wasps), and compared their patterns of molecular evolution to two social bees; Bombus (bumblebees), and Apis (honey bees). This species triad allowed us to study molecular evolution across a gradient of social complexity (Polistes Bombus Apis) and compare species pairs that have similar (i.e. Polistes and Bombus) or different (i.e. Polistes and Apis) life histories, while controlling for phylogenetic distance. We found that regulatory genes have high levels of positive selection in Polistes; consistent with the prediction that adaptive changes in gene regulation are important during early stages of social evolution. Polistes and Bombus exhibit greater similarity in patterns of adaptive evolution including greater overlap of genes experiencing positive selection, and greater positive selection on queen-biased genes. Our findings suggest that either adaptive evolution of a few key genes underlie the evolution of simpler forms of eusociality, or that the initial stages of social evolution lead to selection on a few key traits orchestrated by orthologous genes and networks.