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.

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.

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.

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.