Impacts of neonicotinoid insecticides on bumble bee energy metabolism are revealed under nectar starvation.

Bumble bees are an important group of insects that provide essential pollination services as a consequence of their foraging behaviors. These pollination services are driven, in part, by energetic exchanges between flowering plants and individual bees. Thus, it is important to examine bumble bee energy metabolism and explore how it might be influenced by external stressors contributing to declines in global pollinator populations. Two stressors that are commonly encountered by bees are insecticides, such as the neonicotinoids, and nutritional stress, resulting from deficits in pollen and nectar availability. Our study uses a metabolomic approach to examine the effects of neonicotinoid insecticide exposure on bumble bee metabolism, both alone and in combination with nutritional stress. We hypothesized that exposure to imidacloprid disrupts bumble bee energy metabolism, leading to changes in key metabolites involved in central carbon metabolism. We tested this by exposing Bombus impatiens workers to imidacloprid according to one of three exposure paradigms designed to explore how chronic versus more acute (early or late) imidacloprid exposure influences energy metabolite levels, then also subjecting them to artificial nectar starvation. The strongest effects of imidacloprid were observed when bees also experienced nectar starvation, suggesting a combinatorial effect of neonicotinoids and nutritional stress on bumble bee energy metabolism. Overall, this study provides important insights into the mechanisms underlying the impact of neonicotinoid insecticides on pollinators, and underscores the need for further investigation into the complex interactions between environmental stressors and energy metabolism.

Substances in the mandibular glands mediate queen effects on larval development and colony organization in an annual bumble bee.

Social organization is commonly dynamic, with extreme examples in annual social insects, but little is known about the underlying signals and mechanisms. Bumble bee larvae with close contact to a queen do not differentiate into gynes, pupate at an earlier age, and are commonly smaller than siblings that do not contact a queen. We combined detailed observations, proteomics, microRNA transcriptomics, and gland removal surgery to study the regulation of brood development and division of labor in the annual social bumble bee Bombus terrestris. We found that regurgitates fed to larvae by queens and workers differ in their protein and microRNA composition. The proteome of the regurgitate overlaps significantly with that of the mandibular (MG) and hypopharyngeal glands (HPG), suggesting that these exocrine glands are sources of regurgitate proteins. The proteome of the MG and HPG, but not the salivary glands, differs between queens and workers, with caste-specificity preserved for the MG and regurgitate proteomes. Queens subjected to surgical removal of the MG showed normal behavior, brood care, and weight gain, but failed to shorten larval development. These findings suggest that substances in the queen MG are fed to larvae and influence their developmental program. We suggest that when workers emerge and contribute to larval feeding, they dilute the effects of the queen substances, until she can no longer manipulate the development of all larvae. Longer developmental duration may allow female larvae to differentiate into gynes rather than to workers, mediating the colony transition from the ergonomic to the reproductive phase.

Field-realistic concentrations of a neonicotinoid insecticide influence socially regulated brood development in a bumblebee.

The systemic neonicotinoid insecticides are considered as one of the key culprits contributing to ongoing declines in pollinator health and abundance. Bumblebees are among the most important pollinators of temperate zone plants, making their susceptibility to neonicotinoid exposure of great concern. We report that bumblebee (Bombus terrestris) colonies exposed to field-realistic concentrations of the commonly used neonicotinoid Imidacloprid grew slower, consumed less food, and produced fewer workers, males and gynes, but unexpectedly produced larger workers compared to control colonies. Behavioural observations show that queens in pesticide-treated colonies spend more time inactive and less time caring for the brood. We suggest that the observed effects on brood body size are driven by a decreased queen ability to manipulate the larva developmental programme. These findings reveal an intricate and previously unknown effect of insecticides on the social interactions controlling brood development in social insect colonies. Insecticide influences on the social mechanisms regulating larval development are potentially detrimental for bumblebees, in which body size strongly influences both caste differentiation and the division of labour among workers, two organization principles of insect societies.

Pollen diet mediates how pesticide exposure impacts brain gene expression in nest-founding bumble bee queens.

A primary goal in biology is to understand the effects of multiple, interacting environmental stressors on organisms. Wild and domesticated bees are exposed to a wide variety of interacting biotic and abiotic stressors, with widespread declines in floral resources and agrochemical exposure being two of the most important. In this study, we used examinations of brain gene expression to explore the sublethal consequences of neonicotinoid pesticide exposure and pollen diet composition in nest-founding bumble bee queens. We demonstrate for the first time that pollen diet composition can influence the strength of bumble bee queen responses to pesticide exposure at the molecular level. Specifically, one pollen mixture in our study appeared to buffer bumble bee queens entirely against the effects of pesticide exposure, with respect to brain gene expression. Additionally, we detected unique effects of pollen diet and sustained (versus more temporary) pesticide exposure on queen gene expression. Our findings support the hypothesis that nutritional status can help buffer animals against the harmful effects of other stressors, including pesticides, and highlight the importance of using molecular approaches to explore sublethal consequences of stressors.

Bumble Bee (Bombus vosnesenskii) Queen Nest Searching Occurs Independent of Ovary Developmental Status.

Studies on the physiological states of wild-caught organisms are essential to uncovering the links between ecological and physiological processes. Bumble bee queens emerge from overwintering in the spring. At this time, queens develop their ovaries and search for a nest site in which to start a colony. Whether these two processes, ovary development and nest-searching, interact with or influence one another remains an unresolved question in behavioral physiology. We explored the hypothesis that ovary development and nest-searching might be mechanistically connected, by testing whether (1) ovary development precedes nest-searching behavior; (2) nest occupation precedes ovary development; or (3) ovary development and nest-searching occur independently, in bumble bee (Bombus vosnesenskii) queens. We collected queens either nest-searching (and thus prior to occupying a nest) or pollen-collecting (and thus provisioning an occupied nest) and measured their degree of ovary activation. We further screened these queens for parasites or other symbionts, to identify additional factors that may impact their reproductive success at this time. We found that queens searched for and occupied nests at all stages of ovary development, indicating that these processes occur independently in this system. Nest-searching queens were more likely to have substantial mite loads than pollen-collecting queens, who had already located and occupied a nest. However, mite loads did not significantly predict ovary developmental status. Collectively, our work shows that nesting status and symbionts alone are insufficient to explain the variation in spring bumble bee queen ovary development. We propose that ovary development and nest-searching occur opportunistically, which may enable queens to begin laying eggs earlier in the season than if these processes occurred in discrete succession.

Estudios sobre los estados fisiológicos de los organismos capturados en la naturaleza son esenciales para descubrir los vínculos entre los procesos fisiológicos y ecológicos. Las reinas de abejorro emergen de la hibernación al comienzo de la primavera. En este momento, las reinas desarrollan sus ovarios y buscan un sitio de anidación para iniciar una colonia. Si estos dos procesos, el desarrollo de los ovarios y la búsqueda del nido, interactúan o se influyen mutuamente sigue siendo una cuestión sin resolver en la fisiología del comportamiento. Exploramos la hipótesis de que el desarrollo de los ovarios y la búsqueda de nidos podrían estar mecánicamente conectados, probando si (1) el desarrollo de los ovarios precede al comportamiento de búsqueda del nido; (2) la ocupación del nido precede al desarrollo de los ovarios; o (3) el desarrollo de los ovarios y la búsqueda del nido ocurren de forma independiente, en las reinas de abejorros (Bombus vosnesenskii). Recolectamos reinas que estaban buscando un nido (en proceso de anidación) o recolectando polen (por lo tanto, aprovisionando un nido ya ocupado) y medimos su grado de activación ovárica. Además, examinamos a estas reinas en busca de parásitos u otros simbiontes para identificar factores adicionales que podrían afectar el éxito reproductivo durante este momento. Encontramos que las reinas buscaron y ocuparon nidos en todas las etapas del desarrollo de los ovarios, lo que indica que estos procesos ocurren de manera independiente en este sistema. Las reinas que buscaban un nido eran más propensas a tener cargas sustanciales de ácaros en comparación a las reinas que recolectaban polen, que ya habían localizado y ocupado un nido. Sin embargo, el número de ácaros no está asociados con el desarrollo ovárico. Colectivamente, nuestros datos demuestran que el estado de anidación y los simbiontes por sí solos son insuficientes para explicar la variación en el desarrollo de los ovario de las reinas de abejorro durante la primavera. Proponemos que el desarrollo de los ovarios y la búsqueda de nidos ocurren de manera oportuna, lo cual permitiría que las reinas comenzarán a depositar huevos al inicio de la temporada, comportamiento que no sucedería si estos procesos ocurrieran en una sucesión discreta.

Estudos fisiológicos de organismos não domesticados são essenciais para entender a associação entre os processos ecológicos e fisiológicos. As abelhas rainhas do gênero Bombus emergem durante a primavera após o período de diapausa que ocorre no inverno. Neste momento, as rainhas desenvolvem seus ovários e procuram por um local de nidificação. Nesse contexto, uma questão ainda não resolvida na área de fisiologia comportamental é se haveria uma interação ou influência um ao outro entre esses dois processos, desenvolvimento ovariano e nidificação. Assim, exploramos a hipótese de que o desenvolvimento do ovário e a nidificação podem estar mecanicamente conectados, testando se (1) o desenvolvimento do ovário precede o comportamento de nidificação; (2) a ocupação do ninho precede o desenvolvimento do ovário; ou (3) o desenvolvimento do ovário e a busca de ninhos ocorrem independentemente, em abelhas rainhas de Bombus vosnesenskii. Coletamos abelhas rainhas procurando ninhos (processo de nidificação) ou coletando pólen (portanto, processo de aprovisionamento já iniciado) e medimos o grau de ativação do ovário nessas abelhas. Em seguida, essas rainhas foram inspecionadas para detecção de parasitas ou outros simbiontes, para identificação de fatores adicionais que poderiam afetar o sucesso reprodutivo neste momento. Observamos todos os estágios do desenvolvimento ovariano em ambos os períodos de nidificação e aprovisionamento, indicando que esses processos ocorrem de forma independente nessa espécie. Nossos dados sugerem que abelhas rainhas em busca de ninho são mais susceptíveis a terem cargas substanciais de ácaros do que rainhas no período de aprovisionamento, as quais já ocupavam um ninho. No entanto, a quantidade de ácaros não está associada com desenvolvimento ovariano. Em conjunto, nossos dados demostram que o status de nidificação e os simbiontes são insuficientes para explicar a variação no desenvolvimento do ovário das abelhas rainhas. Sugerimos que o desenvolvimento dos ovários e a nidificação ocorrem de forma oportunista, o que pode permitir que as rainhas comecem a ovipositar antecipadamente sem relação com os processos anteriores.

Convergent Loss of Prothoracicotropic Hormone, A Canonical Regulator of Development, in Social Bee Evolution.

The evolution of insect sociality has repeatedly involved changes in developmental events and their timing. Here, we propose the hypothesis that loss of a canonical regulator of moulting and metamorphosis, prothoracicotropic hormone (PTTH), and its receptor, Torso, is associated with the evolution of sociality in bees. Specifically, we posit that the increasing importance of social influences on early developmental timing in social bees has led to their decreased reliance on PTTH, which connects developmental timing with abiotic cues in solitary insects. At present, the evidence to support this hypothesis includes the absence of genes encoding PTTH and Torso from all fully-sequenced social bee genomes and its presence in all available genomes of solitary bees. Based on the bee phylogeny, the most parsimonious reconstruction of evolutionary events is that this hormone and its receptor have been lost multiple times, across independently social bee lineages. These gene losses shed light on possible molecular and cellular mechanisms that are associated with the evolution of social behavior in bees. We outline the available evidence for our hypothesis, and then contextualize it in light of what is known about developmental cues in social and solitary bees, and the multiple precedences of major developmental changes in social insects.

Mass-flowering monoculture attracts bees, amplifying parasite prevalence.

As the global agricultural footprint expands, it is increasingly important to address the link between the resource pulses characteristic of monoculture farming and wildlife epidemiology. To understand how mass-flowering crops impact host communities and subsequently amplify or dilute parasitism, we surveyed wild and managed bees in a monoculture landscape with varying degrees of floral diversification. We screened 1509 bees from 16 genera in sunflower fields and in non-crop flowering habitat across 200 km2 of the California Central Valley. We found that mass-flowering crops increase bee abundance. Wild bee abundance was subsequently associated with higher parasite presence, but only in sites with a low abundance of non-crop flowers. Bee traits related to higher dispersal ability (body size) and diet breadth (pollen lecty) were also positively related to parasite presence. Our results highlight the importance of non-crop flowering habitat for supporting bee communities. We suggest monoculture alone cannot support healthy bees.

An organizing feature of bumble bee life history: worker emergence promotes queen reproduction and survival in young nests.

Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests.

Flexibility in the Critical Period of Nutrient Sequestration in Bumble Bee Queens.

SYNOPSIS: Bumble bee queens undergo a nutrient storage period prior to entering diapause wherein they sequester glycogen and lipids that are metabolized during overwintering. In the laboratory under optimal food availability conditions, the majority of nutrients are sequestered during the first few days of adulthood. However, if food resources are scarce during this narrow window of time, wild queen bumble bees might be limited in their ability to obtain adequate food resources for overwintering. Here we used a laboratory experiment to examine whether queen bumble bees exhibit flexibility in the timing of pre-overwintering nutrient sequestration, by limiting their access to either nectar (artificial) or pollen, the two primary foods for bumble bees, for varying periods of time. In response to these treatments, we quantified queen survival, changes in weight, and glycogen and lipids levels. We found evidence that queens are able to recuperate almost entirely from food resource limitation, with respect to nutrient storage, especially when it is experienced for shorter durations (up to 6 days). This study sheds light on how bumble bee queens are impacted by food resource availability at a critical life stage. PORTUGUESE: As abelhas rainhas do gênero Bombus armazenam nutrientes antes de entrarem em diapausa, sequestrando o glicogênio e os lipídios que serão metabolizados durante o inverno. Em condições ideais de disponibilidade de alimento no laboratório, a maioria dos nutrientes é sequestrada nos primeiros dias de vida adulta. No entanto, em condições de escassez de alimento na natureza, as rainhas podem sofrer limitações em sua capacidade de obter recursos para o inverno. Nesse contexto, em condições controladas, examinamos se as rainhas exibem variações no sequestro de nutrientes, limitando o acesso ao néctar (artificial) ou pólen, seus principais alimentos, em diferentes intervalos de tempo. Em resposta a esses tratamentos, quantificamos a taxa de sobrevivência das rainhas, as mudanças no peso e os níveis de glicogênio e lipídios. Encontramos evidências de que as rainhas são capazes de recuperar a capacidade de armazenar nutrientes quase inteiramente, especialmente em períodos mais curtos de escassez de alimento (até 6 dias). Este estudo lança luz sobre como as rainhas são afetadas pela variação na disponibilidade de recursos alimentares em um estágio crítico da vida. SPANISH: Las abejas reinas de generó Bombus, mejor conocidas como reinas de abejorro se someten a un período de almacenamiento de nutrientes antes de entrar en diapausa, en el cual secuestran glucógeno y lípidos que se metabolizan durante el invierno. En el laboratorio, en condiciones óptimas de disponibilidad de alimentos, la mayoría de los nutrientes se secuestran durante los primeros días de la edad adulta. Sin embargo, si los recursos alimenticios son escasos durante esta estrecha ventana de tiempo, las abejas reinas silvestres podrían verse limitadas en su capacidad para obtener recursos alimenticios adecuados para pasar el invierno. Aquí utilizamos un experimento de laboratorio para examinar si las abejas reinas exhiben flexibilidad en el momento del secuestro de nutrientes antes de la hibernación, al limitar su acceso al néctar (artificial) o al polen, los dos alimentos principales de los abejorros, durante períodos variables. En respuesta a estos tratamientos, cuantificamos la supervivencia de la reina, los cambios de peso y los niveles de glucógeno y lípidos. Encontramos evidencia de que las reinas pueden recuperarse casi por completo de la limitación de los recursos alimenticios, con respecto al almacenamiento de nutrientes, especialmente cuando se experimenta por períodos más cortos (hasta 6 días). Este estudio arroja luz sobre cómo las abejas reinas se ven afectadas por la disponibilidad de recursos alimenticios en una etapa crítica de la vida.

Care-giver identity impacts offspring development and performance in an annually social bumble bee.

BACKGROUND: The developmental fates of offspring have the potential to be influenced by the identity of their care-givers and by the nature of the care that they receive. In animals that exhibit both parental and alloparental care, such as the annually eusocial insects, the influence of care-giver identity can be directly assessed to yield mechanistic and evolutionary insights into the origins and elaboration of brood care. Here, we performed a comparative investigation of maternal and worker brood care in bumble bees, a pollinator group where mothers (queens) rear the first offspring in the nest, and then daughters (workers) assume this role upon their emergence. Specifically, we compared the effects of queen and worker brood care on offspring development and also offspring performance, for a set of traits related to sensory biology, learning, and stress resistance. RESULTS: We found that queen-reared workers were smaller-bodied than worker-reared offspring, suggesting that bumble bee queens influence body size determination in their offspring. We also found that queen-reared workers were more resistant to starvation, which might be beneficial for early nesting success. These maternal influences could not be explained by feeding rate, given that we detected a similar offspring feeding frequency in both queens and workers. CONCLUSION: Bumble bee queens have a unique influence on the development of the first offspring in the nest, which they rear, relative to worker-reared workers. We propose that bumble bee brood care has been shaped by a suite of evolutionary and ecological factors, which might include a maternal influence on traits that promote survival of incipient colonies.

Transcriptome analysis reveals nutrition- and age-related patterns of gene expression in the fat body of pre-overwintering bumble bee queens.

Many diapausing insects undergo a nutrient storage period prior to their entry into diapause. Bumble bee queens diapause as adults in the winter preceding their spring nest initiation period. Before diapause, they sequester glycogen and lipids, which they metabolize during the overwintering period. We used RNA sequencing to examine how age and nectar diet (specifically, the concentration of sucrose in nectar) impact gene expression in the pre-overwintering bumble bee queen fat body, the "liver-like" organ in insects with broad functions related to nutrient storage and metabolism. We found that diet on its own, and in combination with age, impacts the expression of genes involved in detoxification. Age was also a strong driver of gene expression, especially at earlier ages (up to 3 days). In addition to these molecular correlates of diet and age, we also found a putative molecular signature of diapause entry or preparation in adult queens in the oldest age group (12 days) fed the most sucrose-rich diet, based on comparisons between our data set and another transcriptome data set from bumble bee queens. This transcriptomic pattern suggests that preparation for (or entry into) diapause might be in part mediated by nutritional state in bumble bee queens. Collectively, these findings show that there are molecular processes in the fat body that are responsive to sucrose levels in the diet and/or associated with age-related maturational changes. A better understanding of these processes may shed light on important aspects of bumble bee biology, such as queen responses to nutritional and other forms of stress, and the factors that regulate their entrance into diapause.

Pollen Diet Composition Impacts Early Nesting Success in Queen Bumble Bees Bombus impatiens Cresson(Hymenoptera: Apidae).

Bumble bees are generalist pollinators that typically collect floral rewards from a wide array of flowering plant species. Among the greatest threats to wild bumble bee populations worldwide, many of which are declining, is a loss of floral resource abundance and diversity in the landscapes they inhabit. We examined how composition of pollen diet impacts early nesting success in laboratory-reared queens of the bumble bee Bombus impatiens. Specifically, we provided queens and their young nests with one of three pollen diets, each of which was dominated by a single pollen type, and explored how this diet treatment influenced the length of time until queens initiated nests, total counts of brood in the nest at the end of the experiment (8 wk later), and the size and weight of adult offspring produced. We found that the amount of later-stage brood (pupae and/or adults) produced by recently-initiated nests was strongly impacted by pollen diet. For example, on average 66% fewer later-stage brood were found in nests provided with the Cistus pollen Linnaeus (Cistaceae), relative to the predominantly Asteraceae pollen. This finding suggests that particular pollen diet compositions may delay larval growth, which delays colony development and may ultimately be detrimental for young nests. This study sheds light on how one of the leading stressors for bumble bees (nutritional stress) may negatively impact populations through its influence on brood production during the nest-founding stage of the colony cycle.

Diet and nutritional status during early adult life have immediate and persistent effects on queen bumble bees.

Many insects sequester nutrients during developmentally programmed periods, which they metabolize during subsequent life history stages. During these periods, failure to store adequate nutrients can have persistent effects on fitness. Here, we examined a critical but under-studied nutrient storage period in queen bumble bees: the first days of adult life, which are followed by a diapause period typically coinciding with winter. We experimentally manipulated availability of pollen (the primary dietary source of lipids and protein) and the sugar concentration of artificial nectar (the primary source of carbohydrates) for laboratory-reared queens during this period and examined three nutritional phenomena: (i) diet impacts on nutritional status, (ii) the timescale upon which nutrient sequestration occurs and (iii) the fitness consequences of nutrient sequestration, specifically related to survival across the life cycle. We found evidence that pollen and nectar starvation negatively impact lipid storage, whereas nectar sugar concentration impacts stored carbohydrates. The majority of nutrients were stored during the first ~ 3 days of adult life. Nutrients derived from pollen during this period appear to be more critical for surviving earlier life stages, whereas nutrients sequestered from nectar become more important for surviving the diapause and post-diapause periods. Negative impacts of a poor diet during early life persisted in our experiment, even when pollen and a relatively high (50%) nectar sugar concentration were provided post-diapause. Based on these findings, we posit that the nutritional environment during the early adult life of queens has both immediate and persistent impacts on fitness. These findings underscore the importance of examining effects of stage-specific nutritional limitations on physiology and life history traits in this social insect group. Moreover, the findings may shed light on how declining food resources are contributing to the decline of wild bumble bee populations.

Effects of neonicotinoid insecticide exposure and monofloral diet on nest-founding bumblebee queens.

Bumblebees are among the world's most important groups of pollinating insects in natural and agricultural ecosystems. Each spring, queen bumblebees emerge from overwintering and initiate new nests, which ultimately give rise to workers and new reproductives later in the season. Nest initiation and survival are thus key drivers of both bumblebee pollination services and population dynamics. We performed the first laboratory experiment with the model bumblebee species Bombus impatiens that explores how early nesting success is impacted by the effects of temporary or more sustained exposure to sublethal levels of a neonicotinoid-type insecticide (imidacloprid at 5 ppb in nectar) and by reliance on a monofloral pollen diet, two factors that have been previously implicated in bumblebee decline. We found that queens exhibited increased mortality and dramatically reduced activity levels when exposed to imidacloprid, as well as delayed nest initiation and lower brood numbers in the nest, but partially recovered from these effects when they only received early, temporary exposure. The effects of pollen diet on individual queen- and colony-level responses were overshadowed by effects of the insecticide, although a monofloral pollen diet alone was sufficient to negatively impact brood production. These findings speak to the sensitivity of queen bumblebees during the nest initiation phase of the colony cycle, with implications for how queens and their young nests are uniquely impacted by exposure to threats such as pesticide exposure and foraging habitat unsuitability.

Bumble bee ecophysiology: integrating the changing environment and the organism.

Bumble bees are among the most ecologically and economically important pollinators worldwide, yet many of their populations are being threatened by a suite of interrelated, human-mediated environmental changes. Here, I discuss recent progress in our understanding of bumble bee ecophysiology, including advances related to thermal biology in light of global warming; nutritional biology in the context of declining food resources; and the capacity for bumble bees to exhibit physiological plasticity or adaptations to novel or extreme environments, with reference to their evolutionary history and current biogeography.

Wild bee nutritional ecology: predicting pollinator population dynamics, movement, and services from floral resources.

Pollination services are inherently shaped by floral resource availability, through the mediation of pollinator population dynamics and the influence on energetically costly processes, such as foraging. Here, we review recent insights that have improved our mechanistic understanding of how floral resources shape bee populations and pollination services. Our scope includes advances in our understanding of how individual bees and their populations are shaped by nutrient availability; investigations into how contemporary floral resource landscapes influence foraging; and new insights into how these relationships are indirectly impacted by biotic and abiotic factors across communities and landscapes. Throughout our review, we take a mechanistic, multi-scalar approach that highlights the complexity of interactions between floral resources and bees, across space and time.

Phylogenomics Controlling for Base Compositional Bias Reveals a Single Origin of Eusociality in Corbiculate Bees.

As increasingly large molecular data sets are collected for phylogenomics, the conflicting phylogenetic signal among gene trees poses challenges to resolve some difficult nodes of the Tree of Life. Among these nodes, the phylogenetic position of the honey bees (Apini) within the corbiculate bee group remains controversial, despite its considerable importance for understanding the emergence and maintenance of eusociality. Here, we show that this controversy stems in part from pervasive phylogenetic conflicts among GC-rich gene trees. GC-rich genes typically have a high nucleotidic heterogeneity among species, which can induce topological conflicts among gene trees. When retaining only the most GC-homogeneous genes or using a nonhomogeneous model of sequence evolution, our analyses reveal a monophyletic group of the three lineages with a eusocial lifestyle (honey bees, bumble bees, and stingless bees). These phylogenetic relationships strongly suggest a single origin of eusociality in the corbiculate bees, with no reversal to solitary living in this group. To accurately reconstruct other important evolutionary steps across the Tree of Life, we suggest removing GC-rich and GC-heterogeneous genes from large phylogenomic data sets. Interpreted as a consequence of genome-wide variations in recombination rates, this GC effect can affect all taxa featuring GC-biased gene conversion, which is common in eukaryotes.

Molecular tools and bumble bees: revealing hidden details of ecology and evolution in a model system.

Bumble bees are a longstanding model system for studies on behaviour, ecology and evolution, due to their well-studied social lifestyle, invaluable role as wild and managed pollinators, and ubiquity and diversity across temperate ecosystems. Yet despite their importance, many aspects of bumble bee biology have remained enigmatic until the rise of the genetic and, more recently, genomic eras. Here, we review and synthesize new insights into the ecology, evolution and behaviour of bumble bees that have been gained using modern genetic and genomic techniques. Special emphasis is placed on four areas of bumble bee biology: the evolution of eusociality in this group, population-level processes, large-scale evolutionary relationships and patterns, and immunity and resistance to pesticides. We close with a prospective on the future of bumble bee genomics research, as this rapidly advancing field has the potential to further revolutionize our understanding of bumble bees, particularly in regard to adaptation and resilience. Worldwide, many bumble bee populations are in decline. As such, throughout the review, connections are drawn between new molecular insights into bumble bees and our understanding of the causal factors involved in their decline. Ongoing and potential applications to bumble bee management and conservation are also included to demonstrate how genetics- and genomics-enabled research aids in the preservation of this threatened group.

Molecular heterochrony and the evolution of sociality in bumblebees (Bombus terrestris).

Sibling care is a hallmark of social insects, but its evolution remains challenging to explain at the molecular level. The hypothesis that sibling care evolved from ancestral maternal care in primitively eusocial insects has been elaborated to involve heterochronic changes in gene expression. This elaboration leads to the prediction that workers in these species will show patterns of gene expression more similar to foundress queens, who express maternal care behaviour, than to established queens engaged solely in reproductive behaviour. We tested this idea in bumblebees (Bombus terrestris) using a microarray platform with approximately 4500 genes. Unlike the wasp Polistes metricus, in which support for the above prediction has been obtained, we found that patterns of brain gene expression in foundress and queen bumblebees were more similar to each other than to workers. Comparisons of differentially expressed genes derived from this study and gene lists from microarray studies in Polistes and the honeybee Apis mellifera yielded a shared set of genes involved in the regulation of related social behaviours across independent eusocial lineages. Together, these results suggest that multiple independent evolutions of eusociality in the insects might have involved different evolutionary routes, but nevertheless involved some similarities at the molecular level.

Social regulation of maternal traits in nest-founding bumble bee (Bombus terrestris) queens.

During the nest-founding phase of the bumble bee colony cycle, queens undergo striking changes in maternal care behavior. Early in the founding phase, prior to the emergence of workers in the nest, queens are reproductive and also provision and feed their offspring. However, later in the founding phase, queens reduce their feeding of larvae and become specialized on reproduction. This transition is synchronized with the emergence of workers in the colony, who assume the task of feeding their siblings. Using a social manipulation experiment with the bumble bee Bombus terrestris, we tested the hypothesis that workers regulate the transition from feeding brood to specialization on reproduction in nest-founding bumble bee queens. Consistent with this hypothesis, we found that early-stage nest-founding queens with workers prematurely added to their nests reduce their brood-feeding behavior and increase egg laying, and likewise, late-stage nest-founding queens increase their brood-feeding behavior and decrease egg-laying when workers are removed from their nests. Further, brood-feeding and egg-laying behaviors were negatively correlated. We used Agilent microarrays designed from B. terrestris brain expressed sequenced tags (ESTs) to explore a second hypothesis, that workers alter brain gene expression in nest-founding queens. We found evidence that brain gene expression in nest-founding queens is altered by the presence of workers, with the effect being much stronger in late-stage founding queens. This study provides new insights into how the transition from feeding brood to specialization on reproduction in queen bumble bees is regulated during the nest initiation phase of the colony cycle.