Apidae Research Articles

Pollen Diet Diversity does not Affect Gut Bacterial Communities or Melanization in a Social and Solitary Bee Species.

Pollinators face many stressors, including reduced floral diversity. A low-diversity diet can impair organisms' ability to cope with additional stressors, such as pathogens, by altering the gut microbiome and/or immune function, but these effects are understudied for most pollinators. We investigated the impact of pollen diet diversity on two ecologically and economically important generalist pollinators, the social bumble bee (Bombus impatiens) and the solitary alfalfa leafcutter bee (Megachile rotundata). We experimentally tested the effect of one-, two-, or three-species pollen diets on gut bacterial communities in both species, and the melanization immune response in B. impatiens. Pollen diets included dandelion (Taraxacum officinale), staghorn sumac (Rhus typhina), and hawthorn (Crataegus sp.) alone, each pair-wise combination, or a mix of all three species. We fed bees their diet for 7 days and then dissected out guts and sequenced 16S rRNA gene amplicons to characterize gut bacterial communities. To assess melanization in B. impatiens, we inserted microfilament implants into the bee abdomen and measured melanin deposition on the implant. We found that pollen diet did not influence gut bacterial communities in M. rotundata. In B. impatiens, pollen diet composition, but not diversity, affected gut bacterial richness in older, but not newly-emerged bees. Pollen diet did not affect the melanization response in B. impatiens. Our results suggest that even a monofloral, low-quality pollen diet such as dandelion can support diverse gut bacterial communities in captive-reared adults of these bee species. These findings shed light on the effects of reduced diet diversity on bee health.

WING PHENOTYPIC DIVERSITY IN STINGLESS BEES GENERA (APIDAE: MELIPONINI) FROM ECUADOR AMAZONIA

Native stingless bees, Meliponini, are the only social bees that produce honey in addition to honeybees. These bees have been managed in meliponiculture and for crop pollination. In Ecuador, meliponiculture studies are scarce and limited by the lack of species recognition. Traditionally the taxonomic recognition of the species is based on morphological characteristics. In Hymenoptera, the wing shape has proven to be a valuable tool in combination with traditional characters. Due to this, the wing shape was evaluated for discriminating morphospecies in Ecuador’s Amazonian meliponaries. A total of 127 specimens grouped into six genera were analyzed: Melipona (Melikerria) sp., Melipona (Michmelia) sp1., Melipona (Michmelia) sp2., Tetragonisca sp., Paratrigona sp., Nannotrigona sp., Scaura sp., and Plebeia sp. The most significant differences are located at the vein intersection: cubital and cubital 1 (Cu + Cu1), posterior margin of the marginal cell (r and Rs), and basal and posterior marginal cell (M and Rs).

Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini.

The insect mitogenome is typically a compact circular molecule with highly conserved gene contents. Nonetheless, mitogenome structural variations have been reported in specific taxa, and gene rearrangements, usually the tRNAs, occur in different lineages. Because synapomorphies of mitogenome organizations can provide information for phylogenetic inferences, comparative analyses of mitogenomes have been given increasing attention. However, most studies use a very few species to represent the whole genus, tribe, family, or even order, overlooking potential variations at lower taxonomic levels, which might lead to some incorrect inferences. To provide new insights into mitogenome organizations and their implications for phylogenetic inference, this study conducted comparative analyses for mitogenomes of three social bee tribes (Meliponini, Bombini, and Apini) based on the phylogenetic framework with denser taxonomic sampling at the species and population levels. Comparative analyses revealed that mitogenomes of Apini and Bombini are the typical type, while those of Meliponini show diverse variations in mitogenome sizes and organizations. Large inverted repeats (IRs) cause significant gene rearrangements of protein coding genes (PCGs) and rRNAs in Indo-Malay/Australian stingless bee species. Molecular evolution analyses showed that the lineage with IRs have lower d N/ d S ratios for PCGs than lineages without IRs, indicating potential effects of IRs on the evolution of mitochondrial genes. The finding of IRs and different patterns of gene rearrangements suggested that Meliponini is a hotspot in mitogenome evolution. Unlike conserved PCGs and rRNAs whose rearrangements were found only in the mentioned lineages within Meliponini, tRNA rearrangements are common across all three tribes of social bees, and are significant even at the species level, indicating that comprehensive sampling is needed to fully understand the patterns of tRNA rearrangements, and their implications for phylogenetic inference.

A comparative analysis of foraging route development by bumblebees and honey bees

Many pollinators, such as bees, hummingbirds and bats, use multi-destination routes (traplines) to exploit familiar plant resources. However, it is not clear to what extent the mechanisms underpinning trapline development and optimisation are comparable across species. Here we compared route formation, repeatability and efficiency by foragers of two social bee species, the solo foraging bumblebee Bombus terrestris and the mass foraging honey bee Apis mellifera, in the same laboratory conditions. In a simple routing task (with four artificial flowers), all bumblebees and honey bees developed a route, although honey bees were slower to do so. In a more complex routing task (with six flowers), however, only bumblebees developed a route between the 6 flowers. Honey bees took a longer time to discover all flowers and developed routes between fewer flowers. Comparing bumblebees and honey bees using the same experimental paradigm thus revealed key behavioural differences likely resulting from their contrasting collective foraging strategies.

Chemical Insect Attractants Produced by Flowers of Impatiens spp. (Balsaminaceae) and List of Floral Visitors.

The study of the semiochemicals produced by the flowers of Impatiens spp. is an important topic that may explain the reason for the rapid expansion of some species in this genus. Impatiens L. belongs to the Balsaminaceae family, which includes several species considered to be invasive plants in Europe. This study aimed to characterize the phytochemistry of four naturally occurring plant species in Poland, including three invasive alien taxa (Impatiens parviflora, I. glandulifera, and I. capensis) and one native species (I. noli-tangere). Gas chromatographic techniques were used to assess phytochemical profiles of chemical attractant cues in their pollination biology. We detected differences in the scent profiles of the investigated species. All the examined Impatiens species produce various alcohols, i.e., heptacosanol, octacosanol, aldehydes (e.g., octadecanal, eicosanal, etc.), and fatty acids, as well as long-chain hydrocarbons such as dodecane, tricosane, petacosane, hexacosane, and farnesene. Impatiens parviflora, I. glandulifera, and I. capensis produce geraniol and linalool, which attract members of the Apidae family, including bumblebees and honeybees. Impatiens parviflora also produces linalool-derived monoterpenes (linalool oxide and 8-hydroxylinalool), which are a strong attractant for Diptera; this may clarify why the species is mainly visited and pollinated by syrphid flies. A list of insect visitors to the Impatiens species under study can be found in the article.

Urbanisation reduced body size but potentially improved flight performance in bees and wasps

Urbanisation is a main driver of land-use change, leading to rising in temperatures and fragmentation and reduction of green areas. Bees and wasps, which are important insect groups due to the ecosystem services they provide, may respond to this disturbance via changes in morphological traits which are functionally relevant. To date, studies focusing on this aspect only investigated few social bee species, and often gave contrasting results even at intra-generic level. Here, we studied how body size, wing loading, wing aspect ratio and wing fluctuating asymmetry vary in a social ground-nesting bee (Halictus scabiosae), a solitary hole-nesting bee (Osmia cornuta) and a social paper wasp (Polistes dominula) along an urbanisation gradient within Milan (Italy). By assessing the effects of temperature, green areas fragmentation and vegetation productivity on the above-listed functional traits, we found the three species to variably respond to increasing urbanisation, albeit the driving environmental parameters differed among species. More specifically, smaller individuals were sampled in warmer (for bees) and in less productive (for wasps) areas along the urbanisation gradient. Furthermore, greater wing aspect ratio values were recorded at warmer locations for H. scabiosae, lower wing loading was recorded at more fragmented sites for O. cornuta, and greater wing loading was recorded at locations with greater productivity for P. dominula. H. scabiosae and P. dominula showed greater wing fluctuating asymmetry at more fragmented sites. Although distinct species seemed sensitive to different driving factors, our results point toward a consistent response: smaller body but potentially improved flight performance in more urbanised environments.

Solitary Bees Host More Bacteria and Fungi on Their Cuticle than Social Bees.

Bees come into contact with bacteria and fungi from flowering plants during their foraging trips. The Western honeybee (Apis mellifera) shows a pronounced hygienic behavior with social interactions, while the solitary red mason bee (Osmia bicornis) lacks a social immune system. Since both visit the same floral resources, it is intriguing to speculate that the body surface of a solitary bee should harbor a more complex microbiome than that of the social honeybee. We compared the cuticular microbiomes of A. mellifera (including three European subspecies) and O. bicornis for the first time by bacterial 16S rRNA and fungal ITS gene-based high-throughput amplicon sequencing. The cuticular microbiome of the solitary O. bicornis was significantly more complex than that of the social A. mellifera. The microbiome composition of A. mellifera subspecies was very similar. However, we counted significantly different numbers of fungi and a higher diversity in the honeybee subspecies adapted to warmer climates. Our results suggest that the cuticular microbiome of bees is strongly affected by visited plants, lifestyle and adaptation to temperature, which have important implications for the maintenance of the health of bees under conditions of global change.

Bee Assemblage in the Southern Chihuahuan Desert: The Role of Season, Year, and Trap Color in Abundance.

Recognizing how populations fluctuate over time is a crucial factor in determining the environmental elements affecting population persistence. However, the limited information on wild bee populations complicates the estimation of the impact of anthropogenic threats leading to changes in population size. To address this, we conducted a study capturing and monitoring nine species of wild bees through monthly samplings over four years. Tray traps were placed in permanent plots, and capture records were used to determine population size (N) and density (D). A generalized linear model (GLM) was employed to determine how the use of traps affected bee species captures. The families Apidae and Halictidae represented the most captures. Apis mellifera, the Lasioglossum (Dialictus spp.) complex, and Macrotera sinaloana exhibited the largest number of captures and highest population density. Most species (77.7%) showed a tendency to remain constant over the years and to have a higher number of captures in the spring months. Moreover, yellow traps were the most effective in capturing bee individuals. We suggest that the availability of essential resources and the reduction in environmental stressors positively affected the capture of wild bee populations.

Monitoring metal patterns from urban and agrarian sites using the bumblebee Bombus terrestris as a bioindicator

Honeybees are well-established bioindicators for different types of pollutants. This study aims to establish another species of the Apidae family as a bioindicator, with a distinct behaviour and life cycle. The bumblebee Bombus terrestris was used as a bioindicator for 12 metals. Bumblebee hives were placed at sampling sites in and around the city of Aachen, Germany, and metal concentrations were assessed using ICP-MS. Metal concentrations were compared to those found in honeybees described in the literature. Spatial differences in metal patterns were investigated by comparing two land-use types: urban and agrarian. Seasonal differences were compared by taking samples in spring and summer. All analysed metals were detected above the detection limit and within or even above the concentration range found in honeybees. Significant spatial differences were found for the metalloid B and the metal Cd with higher concentrations at the agrarian sites than the urban sites. Significant seasonal differences were found for 8 metals: Fe, Zn, Cu, Ni, Cd, and As concentrations were higher in summer than in spring, while B and V concentrations were higher in spring. To categorise the results, we applied the honeybee contamination index (HCI) and adapted it to bumblebee purposes. According to the HCI, only one agrarian site showed a high contamination level. This study shows that bumblebees are suitable bioindicators for metals. The obtained data can serve as a first baseline in the establishment of additional monitoring studies or risk assessments.

Influence of social lifestyles on host-microbe symbioses in the bees.

Microbiomes are increasingly recognised as critical for the health of an organism. In eusocial insect societies, frequent social interactions allow for high-fidelity transmission of microbes across generations, leading to closer host-microbe coevolution. The microbial communities of bees with other social lifestyles are less studied, and few comparisons have been made between taxa that vary in social structure. To address this gap, we leveraged a cloud-computing resource and publicly available transcriptomic data to conduct a survey of microbial diversity in bee samples from a variety of social lifestyles and taxa. We consistently recover the core microbes of well-studied corbiculate bees, supporting this method's ability to accurately characterise microbial communities. We find that the bacterial communities of bees are influenced by host location, phylogeny and social lifestyle, although no clear effect was found for fungal or viral microbial communities. Bee genera with more complex societies tend to harbour more diverse microbes, with Wolbachia detected more commonly in solitary tribes. We present a description of the microbiota of Euglossine bees and find that they do not share the "corbiculate core" microbiome. Notably, we find that bacteria with known anti-pathogenic properties are present across social bee genera, suggesting that symbioses that enhance host immunity are important with higher sociality. Our approach provides an inexpensive means of exploring microbiomes of a given taxa and identifying avenues for further research. These findings contribute to our understanding of the relationships between bees and their associated microbial communities, highlighting the importance of considering microbiome dynamics in investigations of bee health.

Climate warming and bumble bee declines: the need to consider sub-lethal heat, carry-over effects, and colony compensation.

Global declines in abundance and diversity of insects are now well-documented and increasingly concerning given the critical and diverse roles insects play in all ecosystems. Habitat loss, invasive species, and anthropogenic chemicals are all clearly detrimental to insect populations, but mounting evidence implicates climate change as a key driver of insect declines globally. Warming temperatures combined with increased variability may expose organisms to extreme heat that exceeds tolerance, potentially driving local extirpations. In this context, heat tolerance limits (e.g., critical thermal maximum, CTmax) have been measured for many invertebrates and are often closely linked to climate regions where animals are found. However, temperatures well below CTmax may also have pronounced effects on insects, but have been relatively less studied. Additionally, many insects with out-sized ecological and economic footprints are colonial (e.g., ants, social bees, termites) such that effects of heat on individuals may propagate through or be compensated by the colony. For colonial organisms, measuring direct effects on individuals may therefore reveal little about population-level impacts of changing climates. Here, we use bumble bees (genus Bombus) as a case study to highlight how a limited understanding of heat effects below CTmax and of colonial impacts and responses both likely hinder our ability to explain past and predict future climate change impacts. Insights from bumble bees suggest that, for diverse invertebrates, predicting climate change impacts will require a more nuanced understanding of the effects of heat exposure and additional studies of carry-over effects and compensatory responses by colonies.

Conserved, yet disruption-prone, gut microbiomes in neotropical bumblebees.

Social bees are an important model for the ecology and evolution of gut microbiomes. These bees harbor ancient, specific, and beneficial gut microbiomes and are crucial pollinators. However, most of the research has concentrated on managed honeybees and bumblebees in the temperate zone. Here we used 16S rRNA gene sequencing to characterize gut microbiomes in wild neotropical bumblebee communities from Colombia. We also analyzed drivers of microbiome structure across our data and previously published data from temperate bumblebees. Our results show that lineages of neotropical bumblebees not only retained their ancient gut bacterial symbionts during dispersal from North America but also are prone to major disruption, a shift that is strongly associated with parasite infection. Finally, we also found that microbiomes are much more strongly structured by host phylogeny than by geography, despite the very different environmental conditions and plant communities in the two regions.

Pesticide Exposure and Effects on Non-Apis Bees.

Bees are essential pollinators of many crops and wild plants, and pesticide exposure is one of the key environmental stressors affecting their health in anthropogenically modified landscapes. Until recently, almost all information on routes and impacts of pesticide exposure came from honey bees, at least partially because they were the only model species required for environmental risk assessments (ERAs) for insect pollinators. Recently, there has been a surge in research activity focusing on pesticide exposure and effects for non-Apis bees, including other social bees (bumble bees and stingless bees) and solitary bees. These taxa vary substantially from honey bees and one another in several important ecological traits, including spatial and temporal activity patterns, foraging and nesting requirements, and degree of sociality. In this article, we review the current evidence base about pesticide exposure pathways and the consequences of exposure for non-Apis bees. We find that the insights into non-Apis bee pesticide exposure and resulting impacts across biological organizations, landscapes, mixtures, and multiple stressors are still in their infancy. The good news is that there are many promising approaches that could be used to advance our understanding, with priority given to informing exposure pathways, extrapolating effects, and determining how well our current insights (limited to very few species and mostly neonicotinoid insecticides under unrealistic conditions) can be generalized to the diversity of species and lifestyles in the global bee community. We conclude that future research to expand our knowledge would also be beneficial for ERAs and wider policy decisions concerning pollinator conservation and pesticide regulation.

Large fitness benefits of social nesting in a small carpenter bee

Abstract Facultatively social insects are an optimal model group for the study of the emergence of cooperation between individuals. Factors influencing the fitness benefits of social nesting are still debated. Nonreproductive subordinates can benefit from indirect fitness benefits due to increasing reproductive success of related individuals or direct fitness benefits due to direct future reproduction. Here, we studied the costs and benefits of social nesting in the small carpenter bee Ceratina albosticta. From demographic data and within-nest relatedness, we obtained key parameters for assessing the fitness of solitary females, social primaries, and social secondaries. C. albosticta were found to usually mate with one male and multiple mating is not common although exists at low frequencies. Social nests usually contain two females, which were found to be related (full sisters), but also some females were unrelated to each other. Patterns of parentage from microsatellite loci revealed that only one female reproduces in social nests. Our results show that relatedness, per capita brood productivity, and offspring survival strongly increase the fitness benefits of social nesting strategies. Social secondaries, when related to the social primaries, have higher inclusive fitness than solitary females, but unrelated social nesting females had no indirect fitness and much reduced inclusive fitness compared to solitary females. Interestingly, average fitness benefits of the social secondary were higher than solitary females. This study provides important empirical data on the costs and benefits of sociality in a facultatively social bee and sets the stage for future comparative studies.

Morphology and temporal evolution of ground-nesting bee burrows created by solitary and social species quantified through X-ray imaging

Most research on wild bees has focused on their role as pollinators, while their importance as soil ecosystem engineers has been largely overlooked, despite the fact that most species nest in the soil. There is limited quantitative knowledge regarding the architecture of nests created by wild bees and the temporal evolution of bee burrows. The aim of this study was to evaluate the feasibility of repeatedly scanning ground-nesting bee nests using X-ray computed tomography to quantify the morphology and temporal evolution of burrow systems created by both solitary and social species. We installed eleven large cylinders at locations with ongoing nesting activity of ground-nesting bees, and repeatedly scanned these soil columns with a medical X-ray scanner over a period of 16 months. From the X-ray images, we extracted bee burrows to visualize and quantitatively characterize their morphology and temporal evolution. The architecture and temporal evolution of burrows strongly differed between the studied social and solitary ground-nesting bee species. Burrows created by the solitary species were simple, linear and unbranched burrows, which were not reused and decayed with time. The burrow systems created by the social species were more complex, with highly branched networks of horizontal and vertical burrows, which increased in complexity and size over time during the bee activity period. The persistence of burrows created by ground-nesting bees varied greatly, with some decaying within a few weeks and others remaining mostly intact for the entire 16-month study period. This study demonstrates the potential of X-ray imaging to provide new insights into the underground life of ground-nesting bees, and highlights the locally important role of ground-nesting bees as soil ecosystem engineers.

Description and validation of an improved method to feed solitary bees (Osmia spp.) known amounts of pesticides

Pesticide exposure is an important driver of bee declines. Laboratory toxicity tests provide baseline information on the potential effects of pesticides on bees, but current risk assessment schemes rely on one species, the highly social honey bee, Apis mellifera, and there is uncertainty regarding the extent to which this species is a suitable surrogate for other pollinators. For this reason, Osmia cornuta and Osmia bicornis have been proposed as model solitary bee species in the EU risk assessment scheme. The use of solitary bees in risk assessment requires the development of new methodologies adjusted to the biology of these species. For example, oral dosing methods used with honey bees cannot be readily applied to solitary bees due to differences in feeding behaviour and social interactions. In this study, we describe the “petal method”, a laboratory feeding method, and validate its use in acute and chronic exposure oral tests with Osmia spp. We conducted five experiments in which we compared the performance of several artificial flowers combining visual and olfactory cues against the petal method, or in which variations of the petal method were confronted. We then use the results of these experiments to optimize the feeding arenas and propose standardized methods for both acute and chronic exposure tests. The petal method provides high levels of feeding success, thus reducing the number of bees needed. It works with a wide variety of petal species and with both female and male Osmia spp., thus ensuring reproducibility across studies. To validate the use of the petal method in ecotoxicology tests, we assess the toxicity of a standard reference insecticide, dimethoate, in O. cornuta adults and determine LD50 values for this species. The petal method should facilitate the inclusion of solitary bees in risk assessment schemes therefore increasing the protection coverage of pesticide regulation.

Preferensi Apis cerana terhadap Konsentrasi Gula dan Jarak Dari Sumber Pakan

Apis cerana honey bees are members of the order Hymenoptera, Family Apidae, Sub Family Apinae and Genus Apis. A. cerana bees need feed in the form of nectar and flower pollen (pollen). When the dry season occurs, the availability of natural food sources is difficult to obtain, so alternative feed for bees is very important and necessary. This study aims to determine the concentration of sugar solution preferred by A. cerana bees, to determine the distance to the preferred feed source for A. cerana bees and to determine the direction of the preferred feed source for A. cerana bees. The method used in this research is the split-split plot experimental method with the main plot is the direction, the sub plot is the distance, and the sub-plot is the sugar concentration. The sugar concentration used was 0%, 15%, 35%, and 50%. The distances used are 1 m, 4 m and 7 m which are located in 4 cardinal directions from the bee colony. The data obtained were analyzed using descriptive statistical methods, conservative non-parametric Kruskal Wallis (KW) using SPSS software. The results of this study were the concentration of sugar preferred by A. cerana bees, namely the concentration of sugar 50%, the distance of the preferred feed source for A. cerana bees from the beehive, namely a distance of 7 m, and the direction of the preferred source of feed by A. cerana bees from the beehive, namely east direction.

Lower secondary school students’ knowledge and understandings of bees

ABSTRACT Bees play a pivotal role in maintaining ecosystems and securing food for humankind. As such, it is crucial to shape a scientific understanding of bees for school students at a young age so as to value and protect the little creatures. This study is intended to identify teenage students’ knowledge and understandings of bees in relation to structures, behaviours, functions, threatening factors and loss of bees, via interviews and a drawing test which were administered to a total of 73 seventh-graders from two classes in a lower secondary school. The findings reveal that some drawn bees’ external structures are most often missing, misplaced and erroneously quantified, suggesting a lack of holistic knowledge of bees’ external structures. A majority of students tend to equate bees with social bees and some barely conceive the messages that certain behaviours of bees communicate. Anthropomorphism is commonly used in representing and formulating their understandings of bees. Students’ statements demonstrate that some unproved and insubstantial factors are deemed as a threat to bees and that their anticipations of the impacts of bee loss are characterised by immediacy and directness. Based on these findings, the sources of their misconceptions and misunderstandings as well as some implications are illuminated in relation to bee teaching in biological education.

Eliciting beekeepers’ preferences for the small hive beetle control policy in Italy: a contingent valuation survey approach

Aethina tumida, commonly known as the small hive beetle (SHB), is a parasite of social bee colonies. In 2014, when the beetle was first detected in the Italian Region of Calabria, the Italian Ministry of Health started an SHB control strategy. Over time, dissatisfaction with the control measures has grown among beekeepers and eroded compliance with the reporting obligations. Our study analyzes Southern Italian beekeepers’ preferences toward alternative SHB control policy. We use a contingent valuation survey to elicit beekeepers' preferences for five alternative control strategies. We find the ex-post biosecurity measure in place reflects in the lowest reporting rate. Our results suggest that implementing the destruction of infested hives only (selective destruction) can be a first, effective step toward enhancing compliance with the reporting obligations. Our findings also suggest that training and extension can be a winning strategy to improve beekeepers’ collaboration with the passive SHB surveillance system.

Reproductive potential shapes the expression of nurse-to-forager transition genes in the workers of stingless bees (Meliponini)

Little is known about the molecular mechanisms that underlie the division of labor in stingless bees. We investigated the expression of a set of candidate genes associated with the nurse-to-forager transition in the honey bee in two stingless bee species, Melipona quadrifasciata and Frieseomelitta varia. These species differ with respect to worker reproduction. The workers of M. quadrifasciata lay trophic and reproductive eggs, but those of F. varia are completely sterile. For M. quadrifasciata nurses, we found elevated vitellogenin (Vg) and low juvenile hormone esterase (jhe) transcript levels in the abdomen, in agreement with their reproductive potential. In F. varia, Vg and methyl farnesoate epoxidase (mfe) transcript levels were high in the heads of foragers, indicating an association with foraging behavior. For malvolio (mvl) and foraging (for), both involved with food search behavior, mvl showed persistent low expression in the head, but increasing levels in the abdomen of both species, speaking against a role in behavioral development. The for transcript levels in F. varia were higher in foragers, both in the head and the abdomen, i.e., consistent with foraging. In M. quadrifasciata, however, for expression was higher in the heads of nurse bees, and, thus, is unlikely to play a role in foraging. The results for the two stingless bee species, in comparison with honey bees and bumble bees, indicate that the degree of worker sterility appears to be the primary factor that shapes the expression pattern of key genes in the life history of social bees.