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.

Generalized Stressors on Hive and Forager Bee Colonies.

Hive-forming bees play an integral role in promoting agricultural sustainability and ecosystem preservation. The recent worldwide decline of several species of bees, and in particular, the honeybee in the United States, highlights the value in understanding possible causes. Over the past decade, numerous mathematical models and empirical experiments have worked to understand the causes of colony stress, with a particular focus on colony collapse disorder. We integrate and enhance major mathematical models of the past decade to create a single, analytically tractable model using a traditional disease modeling framework that incorporates both lethal and sublethal stressors. On top of this synthesis, a major innovation of our model is the generalization of stressor attributes including their transmissibility, impairment level, lethality, duration, and temporal-occurrence. Our model is validated against numerous emergent, biological characteristics and demonstrates that precocious foraging and labor destabilization can produce colony collapse disorder. The thresholds for these phenomena to occur depend on the characteristics and timing of the stressor, thus motivating further empirical and theoretical studies into stressor characteristics.

Diverse communication strategies in bees as a window into adaptations to an unpredictable world.

Communication is a fundamental feature of animal societies and helps their members to solve the challenges they encounter, from exploiting food sources to fighting enemies or finding a new home. Eusocial bees inhabit a wide range of environments and they have evolved a multitude of communication signals that help them exploit resources in their environment efficiently. We highlight recent advances in our understanding of bee communication strategies and discuss how variation in social biology, such as colony size or nesting habits, and ecological conditions are important drivers of variation in communication strategies. Anthropogenic factors, such as habitat conversion, climate change, or the use of agrochemicals, are changing the world bees inhabit, and it is becoming clear that this affects communication both directly and indirectly, for example by affecting food source availability, social interactions among nestmates, and cognitive functions. Whether and how bees adapt their foraging and communication strategies to these changes represents a new frontier in bee behavioral and conservation research.

Survivorship and food consumption of immatures and adults of Apis mellifera and Scaptotrigona bipunctata exposed to genetically modified eucalyptus pollen.

Eucalyptus comprises the largest planted area of cultivated production forest in Brazil. Genetic modification (GM) of eucalyptus can provide additional characteristics for increasing productivity and protecting wood yield, as well as potentially altering fiber for a diversity of industrial uses. However, prior to releasing a new GM plant, risk assessments studies with non-target organisms must be undertaken. Bees are prominent biological models since they play an important role in varied ecosystems, including for Eucalyptus pollination. The main goal of this study was to evaluate whether a novel event (Eucalyptus 751K032), which carries the cp4-epsps gene that encodes the protein CP4-EPSPS and nptII gene that encodes the protein NPTII, might adversely affect honey bees (Apis mellifera) and stingless bees (Scaptotrigona bipunctata). The experiments were performed in southern Brazil, as follows: (i) larvae and adults were separately investigated, (ii) three or four different pollen diets were offered to bees, depending on larval or adult status, and (iii) two biological attributes, i.e., survivorship of larvae and adults and food intake by adults were evaluated. The diets were prepared with pollen from GM Eucalyptus 751K032; pollen from conventional Eucalyptus clone FGN-K, multifloral pollen or pure larval food. The insecticide dimethoate was used to evaluate the sensitivity of bees to toxic substances. Datasets were analyzed with Chi-square test, survival curves and repeated measures ANOVA. Results indicated no evidence of adverse effects of Eucalyptus pollen 751K032 on either honey bees or stingless bees assessed here. Therefore, the main findings suggest that the novel event may be considered harmless to these organisms since neither survivorship nor food consumption by bees were affected by it.

Are Botanical Biopesticides Safe for Bees (Hymenoptera, Apoidea)?

The recent global decline in insect populations is of particular concern for pollinators. Wild and managed bees (Hymenoptera, Apoidea) are of primary environmental and economic importance because of their role in pollinating cultivated and wild plants, and synthetic pesticides are among the major factors contributing to their decline. Botanical biopesticides may be a viable alternative to synthetic pesticides in plant defence due to their high selectivity and short environmental persistence. In recent years, scientific progress has been made to improve the development and effectiveness of these products. However, knowledge regarding their adverse effects on the environment and non-target species is still scarce, especially when compared to that of synthetic products. Here, we summarize the studies concerning the toxicity of botanical biopesticides on the different groups of social and solitary bees. We highlight the lethal and sublethal effects of these products on bees, the lack of a uniform protocol to assess the risks of biopesticides on pollinators, and the scarcity of studies on specific groups of bees, such as the large and diverse group of solitary bees. Results show that botanical biopesticides cause lethal effects and a large number of sublethal effects on bees. However, the toxicity is limited when comparing the effects of these compounds with those of synthetic compounds.

Stingless Bee (Apidae: Apinae: Meliponini) Ecology.

Stingless bees form perennial colonies of honey-making insects. The >600 species of stingless bees, mainly Neotropical, live throughout tropical latitudes. Foragers influence floral biology, plant reproduction, microbe dispersal, and diverse ecosystem functions. As tropical forest residents since the upper Cretaceous, they have had a long evolutionary history without competition from honey bees. Most stingless bees are smaller than any Apis species and recruit nest mates to resources, while their defense strategies exclude stinging behavior but incorporate biting. Stingless bees have diversified ecologically; excel in nesting site selection and mutualisms with plants, arthropods, and microbes; and display opportunism, including co-opting plant defenses. As their biology becomes better known, applications to human endeavors are imposing selective pressures from exploitation and approaches to conservation that entail colony extraction from wildlands. Although some meliponines can adjust to new conditions, their populations shall require tropical diversity for survival and reproduction.

The origin of the stingless bee species described by Frederick Smith from Brazilian specimens brought to the London International Exhibition of 1862

ABSTRACT For a long time, the provenance of the specimens used by Frederick Smith to describe the species of stingless bees from Brazil remained a mystery. The recent digitalization of 19th century publications has made possible to trace the origin of the material brought to the London International Exhibition of 1862 by the Brazilian delegation. We document that the bee specimens showed at the International Exhibition, and that served as type material of the species described by Smith, were collected by Manuel Ferreira Lagos, head of the Zoology section of the Comissão Científica de Exploração, during their stay in Ceará, from 1859 to 1861. Even if late, it is important to give due credit to the Comissão Científica de Exploração, and more specifically to Lagos, for the contribution to the knowledge of the stingless bee fauna from Brazil.

Sociality is a key driver of foraging ranges in bees.

Bees are important pollinators of wild and agricultural plants1,2,3,4,5 and there is increasing evidence that many bee populations decline due to a combination of habitat loss, climate change, pesticides, and other anthropogenic effects.6,7,8,9,10,11 One trait that shapes both their role in plant reproduction12,13 and their exposure to anthropogenic stressors is the distance at which bees forage. It has been suggested that bee sociality14 and diet15 affect bee foraging ranges, but how these traits and their potential interactions drive foraging ranges remains unclear. We analyzed flight distance data from 90 bee species and developed an agent-based model to test how social, dietary, and environmental factors affect foraging ranges. We confirm that bee sociality is positively associated with foraging range, with average-sized social bees foraging up to 3 times farther from the nest than size-matched solitary bees. A comparative analysis of social bees and computer simulations shows that foraging distances increase with colony size, supporting the hypothesis that greater foraging distances are an emergent property of increasing colony sizes in a food-limited environment. Flower constancy and communication, two traits often found in social bees, synergistically increase foraging distances further in many simulated environments. Diet breadth (oligolectic versus polylectic diet), on the other hand, does not appear to affect foraging ranges in solitary bees. Our findings suggest that multiple traits linked to bee sociality explain why social bees have greater foraging ranges. This has implications for predicting pollination services and for developing effective conservation strategies for bees and isolated plant populations.15,16,17,18,19.

Pesticide-induced disturbances of bee gut microbiotas.

Social bee gut microbiotas play key roles in host health and performance. Worryingly, a growing body of literature shows that pesticide exposure can disturb these microbiotas. Most studies examine changes in taxonomic composition in Western honey bee (Apis mellifera) gut microbiotas caused by insecticide exposure. Core bee gut microbiota taxa shift in abundance after exposure but are rarely eliminated, with declines in Bifidobacteriales and Lactobacillus near melliventris abundance being the most common shifts. Pesticide concentration, exposure duration, season and concurrent stressors all influence whether and how bee gut microbiotas are disturbed. Also, the mechanism of disturbance-i.e. whether a pesticide directly affects microbial growth or indirectly affects the microbiota by altering host health-likely affects disturbance consistency. Despite growing interest in this topic, important questions remain unanswered. Specifically, metabolic shifts in bee gut microbiotas remain largely uninvestigated, as do effects of pesticide-disturbed gut microbiotas on bee host performance. Furthermore, few bee species have been studied other than A. mellifera, and few herbicides and fungicides have been examined. We call for these knowledge gaps to be addressed so that we may obtain a comprehensive picture of how pesticides alter bee gut microbiotas, and of the functional consequences of these changes.

Spatial resolution and sensitivity of the eyes of the stingless bee, Tetragonula iridipennis.

Stingless bees are important pollinators in the tropics. The tremendous variation in body size makes them an excellent group to study how miniaturization affects vision and visual behaviours. Using direct measurements and micro-CT, we reconstructed the eye structure, estimated anatomical spatial resolution and optical sensitivity of the stingless bee Tetragonula iridipennis. T. iridipennis is similar in size to the Australian stingless bee Tetragonula carbonaria and is smaller than honeybees. It has correspondingly small eyes (area = 0.56 mm2), few ommatidia (2451 ± 127), large inter-facet (3.0 ± 0.6°) and acceptance angles (2.8°). Theoretical estimates suggest that T. iridipennis has poorer spatial resolution (0.17 cycles degree-1) than honeybees, bumblebees, and T. carbonaria. Its optical sensitivity (0.08 µm2 sr), though higher than expected, is within the range of diurnal bees. This may provide them with greater contrast sensitivity, which is likely more relevant than the absolute sensitivity in this diurnal bee. Behaviourally determined detection thresholds for single targets using y-maze experiments were 11.5° for targets that provide chromatic contrast alone and 9.1° for targets providing chromatic and achromatic contrast. Further studies into microhabitat preferences and behaviour are required to understand how miniaturization influences its visual ecology.

Charles Henry Turner and the cognitive behavior of bees.

Social movements in several countries are stimulating a reconsideration of academic structures and historic figures and promoting reparation and recognition of marginalized and forgotten black scientists. A paradigmatic case in that sense is Charles Henry Turner (1867-1923) who was the first African American to receive a graduate degree at the University of Cincinnati and one of the first in earning a PhD degree of the University of Chicago. He performed numerous experiments on sensory perception, orientation, and mating of solitary and social bees, most of which have been unjustly forgotten despite the fact that they anticipated fundamental concepts of animal cognition. We review these studies and highlight the importance of his ideas for modern views of animal cognition and the study of bee behavior. We conclude that besides his scientific contributions, Turner is an inspiration for scientists fighting against social adversity and prejudices.

Pollen Source Richness May Be a Poor Predictor of Bumblebee (Bombus terrestris) Colony Growth.

Agricultural intensification has drastically altered foraging landscapes for bees, with large-scale crop monocultures associated with floral diversity loss. Research on bumblebees and honeybees has shown individuals feeding on pollen from a low richness of floral sources can experience negative impacts on health and longevity relative to higher pollen source richness of similar protein concentrations. Florally rich landscapes are thus generally assumed to better support social bees. Yet, little is known about whether the effects of reduced pollen source richness can be mitigated by feeding on pollen with higher crude protein concentration, and importantly how variation in diet affects whole colony growth, rearing decisions and sexual production. Studying queen-right bumblebee (Bombus terrestris) colonies, we monitored colony development under a polyfloral pollen diet or a monofloral pollen diet with 1.5-1.8 times higher crude protein concentration. Over 6 weeks, we found monofloral colonies performed better for all measures, with no apparent long-term effects on colony mass or worker production, and a higher number of pupae in monofloral colonies at the end of the experiment. Unexpectedly, polyfloral colonies showed higher mortality, and little evidence of any strategy to counteract the effects of reduced protein; with fewer and lower mass workers being reared, and males showing a similar trend. Our findings (i) provide well-needed daily growth dynamics of queenright colonies under varied diets, and (ii) support the view that pollen protein content in the foraging landscape rather than floral species richness per se is likely a key driver of colony health and success.

Spatial Vision and Visually Guided Behavior in Apidae.

The family Apidae, which is amongst the largest bee families, are important pollinators globally and have been well studied for their visual adaptations and visually guided behaviors. This review is a synthesis of what is known about their eyes and visual capabilities. There are many species-specific differences, however, the relationship between body size, eye size, resolution, and sensitivity shows common patterns. Salient differences between castes and sexes are evident in important visually guided behaviors such as nest defense and mate search. We highlight that Apis mellifera and Bombus terrestris are popular bee models employed in the majority of studies that have contributed immensely to our understanding vision in bees. However, other species, specifically the tropical and many non-social Apidae, merit further investigation for a better understanding of the influence of ecological conditions on the evolution of bee vision.

SEX EXPRESSION, BREEDING SYSTEM AND POLLINATORS OF Piper caldense (PIPERACEAE) IN THE BRAZILIAN ATLANTIC FOREST / Expresión sexual, sistema reproductivo y polinizadores de Piper caldense (Piperaceae) en un bosque Atlántico

ABSTRACT Neotropical Piper species have bisexual flowers. Such reproductive trait is considered basal in this pantropical genus. However, neotropical species having unisexual (staminate) flowers along with bisexual ones have also been reported. Dichogamy is common in the genus, associated with either self-compatibility or -incompatibility, as well as with entomophily. We analyzed a natural population of Piper caldense in a Atlantic Forest area (Viçosa municipality, Minas Gerais state, southeastern Brazil). Preliminary observations indicated that the species produces two flower types. We analyzed flower sex in spikes of 50 plants. We obtained additional information through morphological and anatomical studies and scanning electron microscopy analyses. The longevity and exposure dynamics of stigmatic papillae and the pollen release sequence of all four stamens were investigated to verify the degree of dichogamy. Pollination tests were performed, pollinators were identified and their visitation frequency was recorded. Piper caldense has both bisexual and staminate flowers, each flower type being located on separate spikes. These spikes occurred on the same plant, thus indicating andromonoecy; furthermore, plants having only spikes with staminate flowers were also observed. This gender had not yet been reported to the genus. Gradual and sequential exposure of stigmatic papillae associated with asynchronous pollen release (one stamen a day) resulted in incomplete protogyny. Hand pollination tests showed that the species is self-incompatible. Social bees, mainly Apis mellifera and Melipona spp., were the major pollinator group. Our study reinforces the need to associate morphological analysis with floral biology and indicates future changes in studies addressing reproductive traits associated with the phylogeny of the Piper genus.

RESUMEN Las especies neotropicales de Piper presentan flores bisexuales, condición considerada basal al interior de este género pantropical. Sin embargo, fueron observadas especies neotropicales con flores unisexuales (estaminadas), además de las bisexuales. La dicogamia es común en el género y se encuentra asociada a la autocompatibilidad o incompatibilidad, al igual que la entomofilia. Fue analizada una población natural de Piper caldense en un área de bosque Atlántico (municipio de Viçosa, Minas Gerais, sureste de Brasil). Las observaciones preliminares indicaron que esta especie produce dos tipos florales, para lo cual fue analizada la sexualidad de las flores en 50 espigas a través de estudios morfológicos, anatómicos y análisis con microscopia electrónica de barrido. La longevidad y dinámica de exposición de las papilas estigmáticas y la secuencia de liberación de los granos de polen en los cuatro estambres fueron observados para verificar el grado de dicogamia. El sistema reproductivo se evaluó mediante el test de autopolinización espontánea y polinización abierta. Los visitantes florales fueron identificados y se registró su frecuencia de visita. Piper caldense presenta flores bisexuales y estaminadas, cada tipo floral se encuentra en espigas separadas. Estas espigas se encuentran en la misma planta, lo que indica que es andromonoica; adicionalmente, fueron observadas plantas que solo presentaban espigas con flores estaminadas, lo que se constituye en una combinación sexual inédita para el género. La exposición gradual y secuencial de las papilas estigmáticas asociada con la liberación asincrónica de los granos de polen (un estambre por día) indica una protoginia incompleta. Los test de polinización mostraron que la especie es autoincompatible. Las abejas sociales, principalmente Apis mellifera y Melipona spp., fueron los polinizadores principales. Este estudio refuerza la necesidad de asociar los analisis morfológicos con la funcionalidad de las estructuras florales, además indica los cambios futuros en estudios que abordan características reproductivas asociadas a la filogenia de las especies de Piper.

Epigenetic modifications and their relation to caste and sex determination and adult division of labor in the stingless bee Melipona scutellaris

Abstract Stingless bees of the genus Melipona, have long been considered an enigmatic case among social insects for their mode of caste determination, where in addition to larval food type and quantity, the genotype also has a saying, as proposed over 50 years ago by Warwick E. Kerr. Several attempts have since tried to test his Mendelian two-loci/two-alleles segregation hypothesis, but only recently a single gene crucial for sex determination in bees was evidenced to be sex-specifically spliced and also caste-specifically expressed in a Melipona species. Since alternative splicing is frequently associated with epigenetic marks, and the epigenetic status plays a major role in setting the caste phenotype in the honey bee, we investigated here epigenetic chromatin modification in the stingless bee Melipona scutellaris. We used an ELISA-based methodology to quantify global methylation status and western blot assays to reveal histone modifications. The results evidenced DNA methylation/demethylation events in larvae and pupae, and significant differences in histone methylation and phosphorylation between newly emerged adult queens and workers. The epigenetic dynamics seen in this stingless bee species represent a new facet in the caste determination process in Melipona bees and suggest a possible mechanism that is likely to link a genotype component to the larval diet and adult social behavior of these bees.