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In temperate climates, honey bees show strong phenotypic plasticity associated with seasonal changes. In summer, worker bees typically only survive for about a month and can be further classified as young nurse bees (which feed the developing brood) and older forager bees. In winter, brood production and foraging halts and the worker bees live several months. These differences in task and longevity are reflected in their physiology, with summer nurses and long-lived winter bees typically having larger fat bodies, high expression levels of vitellogenin (a longevity, nutrition, and immune-related gene), and larger provisioning glands in their head. The environmental factors (both within the colony and within the surrounding environment) that trigger this transition to long-lived winter bees are poorly understood. One theory suggests is that winter bees are an extended nurse bee state, brought on by a reduction in nursing duties in the fall (i.e., lower brood area). We examine that theory here by assessing nurse bee physiology in both the summer and fall, in colonies with varying levels of brood. We find that season is a better predictor of nurse bee physiology than brood area. This finding suggests that seasonal factors beyond brood area, such as pollen availability and colony demography, may be necessary for inducing the winter bee phenotype. This finding furthers our understanding of winter bee biology, which could have important implications for colony management for winter, a critical period for colony survival.

Pollinators are an essential component of terrestrial food webs and agricultural systems but are threatened by insufficient access to floral resources. Managed honey bees, as generalist foragers that hoard nectar as honey, can act as bioindicators of floral resources available to pollinators in a given landscape through their accumulation of honey. Honey yields across the United States have decreased appreciably since the 1990s, concurrent with shifts in climate, land-use, and large-scale pesticide application. While many factors can affect honey accumulation, this suggests that anthropogenic stressors may be having large-scale impacts on the floral resources that pollinators depend on for their nutrition. We used hierarchical partitioning on five decades of state-level data to parse the most important environmental factors and likely mechanisms associated with spatial and temporal variation in honey yields across the US. Climatic conditions and soil productivity were among the most important variables for estimating honey yields, with states in warm or cool regions with productive soils having the highest honey yields per colony. These findings suggest that foundational factors constrain pollinator habitat suitability and define ecoregions of low or high honey production. The most important temporally varying factors were change in herbicide use, land use (i.e. increase in intensive agriculture and reduction in land conservation programs that support pollinators) and annual weather anomalies. This study provides insights into the interplay between broad abiotic conditions and fine temporal variation on habitat suitability for honey bees and other pollinators. Our results also provide a baseline for investigating how these factors influence floral resource availability, which is essential to developing strategies for resilient plant–pollinator communities in the face of global change.

Conflict between genes inherited from the mother (matrigenes) and the father (patrigenes) is predicted to arise during social interactions among offspring if these genes are not evenly distributed among offspring genotypes. This intragenomic conflict drives parent-specific transcription patterns in offspring resulting from parent-specific epigenetic modifications. Previous tests of the kinship theory of intragenomic conflict in honey bees (Apis mellifera) provided evidence in support of theoretical predictions for variation in worker reproduction, which is associated with extreme variation in morphology and behavior. However, more subtle behaviors – such as aggression – have not been extensively studied. Additionally, the canonical epigenetic mark (DNA methylation) associated with parent-specific transcription in plant and mammalian model species does not appear to play the same role as in honey bees, and thus the molecular mechanisms underlying intragenomic conflict in this species is an open area of investigation. Here, we examined the role of intragenomic conflict in shaping aggression in honey bee workers through a reciprocal cross design and Oxford Nanopore direct RNA sequencing. We attempted to probe the underlying regulatory basis of this conflict through analyses of parent-specific RNA m6A and alternative splicing patterns. We report evidence that intragenomic conflict occurs in the context of honey bee aggression, with increased paternal and maternal allele-biased transcription in aggressive compared to non-aggressive bees, and higher paternal allele-biased transcription overall. However, we found no evidence to suggest that RNA m6A or alternative splicing mediate intragenomic conflict in this species.

Wild and managed pollinators are essential to food production and the function of natural ecosystems; however, their populations are threatened by multiple stressors including pesticide use. Because pollinator species can travel hundreds to thousands of meters to forage, recent research has stressed the importance of evaluating pollinator decline at the landscape scale. However, scientists’ and conservationists’ ability to do this has been limited by a lack of accessible data on pesticide use at relevant spatial scales and in toxicological units meaningful to pollinators. Here, we synthesize information from several large, publicly available datasets on pesticide use patterns, land use, and toxicity to generate novel datasets describing pesticide use by active ingredient (kg, 1997–2017) and aggregate insecticide load (kg and honey bee lethal doses, 1997–2014) for state-crop combinations in the contiguous U.S. Furthermore, by linking pesticide datasets with land-use data, we describe a method to map pesticide indicators at spatial scales relevant to pollinator research and conservation.

Different genes show different levels of expression variability. For example, highly expressed genes tend to exhibit less expression variability. Genes whose promoters have TATA box and initiator motifs tend to have increased expression variability. On the other hand, DNA methylation of transcriptional units, or gene body DNA methylation, is associated with reduced gene expression variability in many species. Interestingly, some insect lineages, most notably Diptera including the canonical model insect Drosophila melanogaster, have lost DNA methylation. Therefore, it is of interest to determine whether genomic features similarly influence gene expression variability in lineages with and without DNA methylation. We analyzed recently generated large-scale data sets in D. melanogaster and honey bee (Apis mellifera) to investigate these questions. Our analysis shows that increased gene expression levels are consistently associated with reduced expression variability in both species, while the presence of TATA box is consistently associated with increased gene expression variability. In contrast, initiator motifs and gene lengths have weak effects limited to some data sets. Importantly, we show that a sequence characteristics indicative of gene body DNA methylation is strongly and negatively associate with gene expression variability in honey bees, while it shows no such association in D. melanogaster. These results suggest the evolutionary loss of DNA methylation in some insect lineages has reshaped the molecular mechanisms concerning the regulation of gene expression variability.

Behavioural variation is essential for animals to adapt to different social and environmental conditions. The Kinship Theory of Intragenomic Conflict (KTIC) predicts that parent‐specific alleles can support different behavioural strategies to maximize allele fitness. Previous studies, including in honey bees (Apis mellifera), supported predictions of the KTIC for parent‐specific alleles to promote selfish behaviour. Here, we test the KTIC prediction that for altruism‐promoting genes (i.e. those that promote behaviours that support the reproductive fitness of kin), the allele with the higher altruism optimum should be selected to be expressed while the other is silenced. In honey bee colonies, workers act altruistically when tending to the queen by performing a ‘retinue’ behaviour, distributing the queen's mandibular pheromone (QMP) throughout the hive. Workers exposed to QMP do not activate their ovaries, ensuring they care for the queen's brood instead of competing to lay unfertilized eggs. Due to the haplodiploid genetics of honey bees, the KTIC predicts that response to QMP is favoured by the maternal genome. We report evidence for parent‐of‐origin effects on the retinue response behaviour, ovarian development and gene expression in brains of worker honey bees exposed to QMP, consistent with the KTIC. Additionally, we show enrichment for genes with parent‐of‐origin expression bias within gene regulatory networks associated with variation in bees' response to QMP. Our study demonstrates that intragenomic conflict can shape diverse social behaviours and influence expression patterns of single genes as well as gene networks.

Each year, millions of kilograms of insecticides are applied to crops in the US. While insecticide use supports food, fuel, and fiber production, it can also threaten non-target organisms, a concern underscored by mounting evidence of widespread decline of pollinator populations. Here, we integrate several public datasets to generate county-level annual estimates of total ‘bee toxic load’ (honey bee lethal doses) for insecticides applied in the US between 1997–2012, calculated separately for oral and contact toxicity. To explore the underlying components of the observed changes, we divide bee toxic load into extent (area treated) and intensity (application rate x potency). We show that while contact-based bee toxic load remained relatively steady, oral-based bee toxic load increased roughly 9-fold, with reductions in application rate outweighed by disproportionate increases in potency (toxicity/kg) and extent. This pattern varied markedly by region, with the greatest increase seen in Heartland (121-fold increase), likely driven by use of neonicotinoid seed treatments in corn and soybean. In this “potency paradox”, farmland in the central US has become more hazardous to bees despite lower volumes of insecticides applied, raising concerns about insect conservation and highlighting the importance of integrative approaches to pesticide use monitoring.