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Müllerian mimicry was proposed to be an example of a coevolved mutualism promoted by population isolation in glacial refugia. This, however, has not been well supported in butterfly models. Here, we use genomic data to test this theory while examining the population genetics behind mimetic diversification in a pair of co-mimetic bumble bees, Bombus breviceps Smith and Bombus trifasciatus Smith. In both lineages, populations were structured by geography but not as much by color pattern, suggesting sharing of color alleles across regions of restricted gene flow and formation of mimicry complexes in the absence of genetic differentiation. Demographic analyses showed mismatches between historical effective population size changes and glacial cycles, and niche modeling revealed only mild habitat retraction during glaciation. Moreover, mimetic subpopulations of the same color form in the two lineages only in some cases exhibit similar population history and genetic divergence. Therefore, the current study supports a more complex history in this comimicry than a simple refugium-coevolution model.

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Müllerian mimicry provides natural replicates ideal for exploring mechanisms underlying adaptive phenotypic divergence and convergence, yet the genetic mechanisms underlying mimetic variation remain largely unknown. The current study investigates the genetic basis of mimetic color pattern variation in a highly polymorphic bumble bee, Bombus breviceps (Hymenoptera, Apidae). In South Asia, this species and multiple comimetic species converge onto local Müllerian mimicry patterns by shifting the abdominal setal color from orange to black. Genetic crossing between the orange and black phenotypes suggested the color dimorphism being controlled by a single Mendelian locus, with the orange allele being dominant over black. Genome-wide association suggests that a locus at the intergenic region between 2 abdominal fate-determining Hox genes, abd-A and Abd-B, is associated with the color change. This locus is therefore in the same intergenic region but not the same exact locus as found to drive red black midabdominal variation in a distantly related bumble bee species, Bombus melanopygus. Gene expression analysis and RNA interferences suggest that differential expression of an intergenic long noncoding RNA between abd-A and Abd-B at the onset setal color differentiation may drive the orange black color variation by causing a homeotic shift late in development. Analysis of this same color locus in comimetic species reveals no sequence association with the same color shift, suggesting that mimetic convergence is achieved through distinct genetic routes. Our study establishes Hox regions as genomic hotspots for color pattern evolution in bumble bees and demonstrates how pleiotropic developmental loci can drive adaptive radiations in nature.

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Globally, insects have been impacted by climate change, with bumble bees in particular showing range shifts and declining species diversity with global warming. This suggests heat tolerance is a likely factor limiting the distribution and success of these bees. Studies have shown high intraspecific variance in bumble bee thermal tolerance, suggesting biological and environmental factors may be impacting heat resilience. Understanding these factors is important for assessing vulnerability and finding environmental solutions to mitigate effects of climate change. In this study, we assess whether geographic range variation in bumble bees in the eastern United States is associated with heat tolerance and further dissect which other biological and environmental factors explain variation in heat sensitivity in these bees. We examine heat tolerance by caste, sex, and rearing condition (wild/lab) across six eastern US bumble bee species, and assess the role of age, reproductive status, body size, and interactive effects of humidity and temperature on thermal tolerance in Bombus impatiens. We found marked differences in heat tolerance by species that correlate with each species' latitudinal range, habitat, and climatic niche, and we found significant variation in thermal sensitivity by caste and sex. Queens had considerably lower heat tolerance than workers and males, with greater tolerance when queens would first be leaving their natal nest, and lower tolerance after ovary activation. Wild bees tended to have higher heat tolerance than lab reared bees, and body size was associated with heat tolerance only in wild-caught foragers. Humidity showed a strong interaction with heat effects, pointing to the need to regulate relative humidity in thermal assays and consider its role in nature. Altogether, we found most tested biological conditions impact thermal tolerance and highlight the stages of these bees that will be most sensitive to future climate change.

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Climate change poses a threat to organisms across the world, with cold-adapted species such as bumble bees (Bombus spp.) at particularly high risk. Understanding how organisms respond to extreme heat events associated with climate change as well as the factors that increase resilience or prime organisms for future stress can inform conservation actions. We investigated the effects of heat stress within different contexts (duration, periodicity, with and without access to food, and in the laboratory versus field) on bumble bee (Bombus impatiens) survival and heat tolerance. We found that both prolonged (5 h) heat stress and nutrition limitation were negatively correlated with worker bee survival and thermal tolerance. However, the effects of these acute stressors were not long lasting (no difference in thermal tolerance among treatment groups after 24 h). Additionally, intermittent heat stress, which more closely simulates the forager behavior of leaving and returning to the nest, was not negatively correlated with worker thermal tolerance. Thus, short respites may allow foragers to recover from thermal stress. Moreover, these results suggest there is no priming effect resulting from short- or long-duration exposure to heat - bees remained equally sensitive to heat in subsequent exposures. In field-caught bumble bees, foragers collected during warmer versus cooler conditions exhibited similar thermal tolerance after being allowed to recover in the lab for 16 h. These studies offer insight into the impacts of a key bumble bee stressor and highlight the importance of recovery duration, stressor periodicity and context on bumble bee thermal tolerance outcomes.

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Vairimorpha, a microsporidian parasite (previously classified as Nosema), has been implicated in the decline of wild bumble bee species in North America. Previous studies examining its influence on colony performance have displayed variable results, from extremely detrimental effects to no observable influence, and little is known about the effects it has on individuals during the winter diapause, a bottleneck for survival in many annual pollinators. Here, we examined the effect of Vairimorpha infection, body size, and mass on diapause survival in Bombus griseocollis gynes. We demonstrate that gyne survival length in diapause is negatively affected by symptomatic Vairimorpha infection of the maternal colony but does not correlate with individual pathogen load. Our findings further indicate that increased body mass offers a protective effect against mortality during diapause in infected, but not in healthy, gynes. This suggests that access to adequate nutritional resources prior to diapause might offset the harmful effect of Vairimorpha infection.

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Bumble bees (Hymenoptera: Apidae, Bombus Latreille) perform important ecological services in both managed and natural ecosystems. Anthropogenically induced change has altered floral resources, climate, and insecticide exposure, factors that impact health and disease levels in these bees. Habitat management presents a solution for improving bee health and biodiversity, but this requires better understanding of how different pathogens and bee species respond to habitat conditions. We take advantage of the washboard of repeated ridges (forested) and valleys (mostly developed) in central Pennsylvania to examine whether local variation in habitat type and other landscape factors influence bumble bee community composition and levels of 4 leading pathogens in the common eastern bumble bee, Bombus impatiens Cresson. Loads of viruses (DWV and BQCV) were found to be lowest in forest habitats, whereas loads of a gut parasite, Crithidia bombi, were highest in forests. Ridgetop forests hosted the most diverse bumble bee communities, including several habitat specialists. B. impatiens was most abundant in valleys, and showed higher incidence in areas of greater disturbance, including more developed, unforested, and lower floral resource sites, a pattern which mirrors its success in the face of anthropogenic change. Additionally, DNA barcoding revealed that B. sandersoni is much more common than is apparent from databases. Our results provide evidence that habitat type can play a large role in pathogen load dynamics, but in ways that differ by pathogen type, and point to a need for consideration of habitat at both macro-ecological and local spatial scales.

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Landscape transcriptomics is an emerging field studying how genome-wide expression patterns reflect dynamic landscape-scale environmental drivers, including habitat, weather, climate, and contaminants, and the subsequent effects on organismal function. This field is benefitting from advancing and increasingly accessible molecular technologies, which in turn are allowing the necessary characterization of transcriptomes from wild individuals distributed across natural landscapes. This research is especially important given the rapid pace of anthropogenic environmental change and potential impacts that span levels of biological organization. We discuss three major themes in landscape transcriptomic research: connecting transcriptome variation across landscapes to environmental variation, generating and testing hypotheses about the mechanisms and evolution of transcriptomic responses to the environment, and applying this knowledge to species conservation and management. We discuss challenges associated with this approach and suggest potential solutions. We conclude that landscape transcriptomics has great promise for addressing fundamental questions in organismal biology, ecology, and evolution, while providing tools needed for conservation and management of species.

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The morphology of insect-induced galls contributes to defences of the gall-inducing insect species against its natural enemies. In terms of gall chemistry, the only defensive compounds thus far identified in galls are tannins that accumulate in many galls, preventing damage by herbivores. Intrigued by the fruit-like appearance of the translucent oak gall (TOG; Amphibolips nubilipennis, Cynipidae, Hymenoptera) induced on red oak (Quercus rubra), we hypothesized that its chemical composition may deviate from other galls. We found that the pH of the gall is between 2 and 3, making it among the lowest pH levels found in plant tissues. We examined the organic acid content of TOG and compared it to fruits and other galls using high-performance liquid chromatography and gas chromatography-mass spectrometry. Malic acid, an acid with particularly high abundance in apples, represents 66% of the organic acid detected in TOGs. The concentration of malic acid was two times higher than in other galls and in apples. Gall histology showed that the acid-containing cells were enlarged and vacuolized just like fruits mesocarp cells. Accumulation of organic acid in gall tissues is convergent with fruit morphology and may constitute a new defensive strategy against predators and parasitoids.

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Bumble bees are characterized by their thick setal pile that imparts aposematic color patterns often used for species-level identification. Like all bees, the single-celled setae of bumble bees are branched, an innovation thought important for pollen collection. To date no studies have quantified the types of setal morphologies and their distribution on these bees, information that can facilitate understanding of their adaptive ecological function. This study defines several major setal morphotypes in the common eastern bumble bee Bombus impatiens Cresson, revealing these setal types differ by location across the body. The positions of these types of setae are similar across individuals, castes, and sexes within species. We analyzed the distribution of the two most common setal types (plumose and spinulate) across the body dorsum of half of the described bumble bee species. This revealed consistently high density of plumose (long-branched) setae across bumble bees on the head and mesosoma, but considerable variation in the amount of metasomal plumosity. Variation on the metasoma shows strong phylogenetic signal at subgeneric and smaller group levels, making it a useful trait for species delimitation research, and plumosity has increased from early Bombus ancestors. The distribution of these setal types suggests these setae may serve several functions, including pollen-collecting and thermoregulatory roles, and probable mechanosensory functions. This study further examines how and when setae of the pile develop, evidence for mechanosensory function, and the timing of pigmentation as a foundation for future genetic and developmental research in these bees.

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Global changes are severely affecting pollinator insect communities worldwide, resulting in repeated patterns of species extirpations and extinctions. Whilst negative population trends within this functional group have understandably received much attention in recent decades, another facet of global changes has been overshadowed: species undergoing expansion. Here, we review the factors and traits that have allowed a fraction of the pollinating entomofauna to take advantage of global environmental change. Sufficient mobility, high resistance to acute heat stress, and inherent adaptation to warmer climates appear to be key traits that allow pollinators to persist and even expand in the face of climate change. An overall flexibility in dietary and nesting requirements is common in expanding species, although niche specialization can also drive expansion under specific contexts. The numerous consequences of wild and domesticated pollinator expansions, including competition for resources, pathogen spread, and hybridization with native wildlife, are also discussed. Overall, we show that the traits and factors involved in the success stories of expanding pollinators are mostly species specific and context dependent, rendering generalizations of 'winning traits' complicated. This work illustrates the increasing need to consider expansion and its numerous consequences as significant facets of global changes and encourages efforts to monitor the impacts of expanding insect pollinators, particularly exotic species, on natural ecosystems.

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The Ichneumonoidea (Ichneumonidae and Braconidae) is an incredibly diverse superfamily of parasitoid wasps that includes species that produce virus-like entities in their reproductive tracts to promote successful parasitism of host insects. Research on these entities has traditionally focused upon two viral genera Bracovirus (in Braconidae) and Ichnovirus (in Ichneumonidae). These viruses are produced using genes known collectively as endogenous viral elements (EVEs) that represent historical, now heritable viral integration events in wasp genomes. Here, new genome sequence assemblies for 11 species and 6 publicly available genomes from the Ichneumonoidea were screened with the goal of identifying novel EVEs and characterizing the breadth of species in lineages with known EVEs. Exhaustive similarity searches combined with the identification of ancient core genes revealed sequences from both known and novel EVEs. One species harbored a novel, independently derived EVE related to a divergent large double-stranded DNA (dsDNA) virus that manipulates behavior in other hymenopteran species. Although bracovirus or ichnovirus EVEs were identified as expected in three species, the absence of ichnoviruses in several species suggests that they are independently derived and present in two younger, less widespread lineages than previously thought. Overall, this study presents a novel bioinformatic approach for EVE discovery in genomes and shows that three divergent virus families (nudiviruses, the ancestors of ichnoviruses, and Leptopilina boulardi Filamentous Virus-like viruses) are recurrently acquired as EVEs in parasitoid wasps. Virus acquisition in the parasitoid wasps is a common process that has occurred in many more than two lineages from a diverse range of arthropod-infecting dsDNA viruses.

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A major goal of evolutionary genetics and evo-devo is to understand how changes in genotype manifest as changes in phenotype. Bumble bees display remarkable color pattern diversity while converging onto numerous regional Müllerian mimicry patterns, thus enabling exploration of the genetic mechanisms underlying convergent phenotypic evolution. In western North America, multiple bumble bee species converge onto local mimicry patterns through parallel shifts of midabdominal segments from red to black. It was previously demonstrated that a Hox gene, Abd-B, is the key regulator of the phenotypic switch in one of these species, Bombus melanopygus, however, the mechanism by which Abd-B regulates color differentiation remains unclear. Using tissue/stage-specific transcriptomic analysis followed by qRT-PCR validation, this study reveals a suite of genes potentially involved downstream of Abd-B during color pattern differentiation. The data support differential genes expression of not only the first switch gene Abd-B, but also an intermediate developmental gene nubbin, and a whole suite of downstream melanin and redox genes that together reinforce the observed eumelanin (black)-pheomelanin (red) ratios. These include potential genes involved in the production of insect pheomelanins, a pigment until recently not thought to occur in insects and thus lacking known regulatory enzymes. The results enhance understanding of pigmentation gene networks involved in bumble bee color pattern development and diversification, while providing insights into how upstream regulators such as Hox genes interact with downstream morphogenic players to facilitate this adaptive phenotypic radiation.

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Bumble bees exhibit exceptional diversity in their segmental body coloration largely as a result of mimicry. In this study we sought to discover genes involved in this variation through studying a lab-generated mutant in bumble bee Bombus terrestris, in which the typical black coloration of the pleuron, scutellum, and first metasomal tergite is replaced by yellow, a color variant also found in sister lineages to B. terrestris. Utilizing a combination of RAD-Seq and whole-genome re-sequencing, we localized the color-generating variant to a single SNP in the protein-coding sequence of transcription factor cut. This mutation generates an amino acid change that modifies the conformation of a coiled-coil structure outside DNA-binding domains. We found that all sequenced Hymenoptera, including sister lineages, possess the non-mutant allele, indicating different mechanisms are involved in the same color transition in nature. Cut is important for multiple facets of development, yet this mutation generated no noticeable external phenotypic effects outside of setal characteristics. Reproductive capacity was reduced, however, as queens were less likely to mate and produce female offspring, exhibiting behavior similar to that of workers. Our research implicates a novel developmental player in pigmentation, and potentially caste, thus contributing to a better understanding of the evolution of diversity in both of these processes.

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Search results from local alignment search tools use statistical scores that are sensitive to the size of the database to report the quality of the result. For example, NCBI BLAST reports the best matches using similarity scores and expect values (i.e., e-values) calculated against the database size. Given the astronomical growth in genomics data throughout a genomic research investigation, sequence databases grow as new sequences are continuously being added to these databases. As a consequence, the results (e.g., best hits) and associated statistics (e.g., e-values) for a specific set of queries may change over the course of a genomic investigation. Thus, to update the results of a previously conducted BLAST search to find the best matches on an updated database, scientists must currently rerun the BLAST search against the entire updated database, which translates into irrecoverable and, in turn, wasted execution time, money, and computational resources. To address this issue, we devise a novel and efficient method to redeem past BLAST searches by introducing iBLAST. iBLAST leverages previous BLAST search results to conduct the same query search but only on the incremental (i.e., newly added) part of the database, recomputes the associated critical statistics such as e-values, and combines these results to produce updated search results. Our experimental results and fidelity analyses show that iBLAST delivers search results that are identical to NCBI BLAST at a substantially reduced computational cost, i.e., iBLAST performs (1 + δ)/δ times faster than NCBI BLAST, where δ represents the fraction of database growth. We then present three different use cases to demonstrate that iBLAST can enable efficient biological discovery at a much faster speed with a substantially reduced computational cost.

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As hybrid zones exhibit selective patterns of gene flow between otherwise distinct lineages, they can be especially valuable for informing processes of microevolution and speciation. The bumble bee, Bombus melanopygus, displays two distinct color forms generated by Müllerian mimicry: a northern "Rocky Mountain'' color form with ferruginous mid-abdominal segments (B. m. melanopygus) and a southern "Pacific'' form with black mid-abdominal segments (B. m. edwardsii). These morphs meet in a mimetic transition zone in northern California and southern Oregon that is more narrow and transitions further west than comimetic bumble bee species. To understand the historical formation of this mimicry zone, we assessed color distribution data for B. melanopygus from the last 100 years. We then examined gene flow among the color forms in the transition zone by comparing sequences from mitochondrial COI barcode sequences, color-controlling loci, and the rest of the nuclear genome. These data support two geographically distinct mitochondrial haplogroups aligned to the ancestrally ferruginous and black forms that meet within the color transition zone. This clustering is also supported by the nuclear genome, which, while showing strong admixture across individuals, distinguishes individuals most by their mitochondrial haplotype, followed by geography. These data suggest the two lineages most likely were historically isolated, acquired fixed color differences, and then came into secondary contact with ongoing gene flow. The transition zone, however, exhibits asymmetries: mitochondrial haplotypes transition further south than color pattern, and both transition over shorter distances in the south. This system thus demonstrates alternative patterns of gene flow that occur in contact zones, presenting another example of mito-nuclear discordance. Discordant gene flow is inferred to most likely be driven by a combination of mimetic selection, dominance effects, and assortative mating.

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Ichneumonoidea is one of the most diverse lineages of animals on the planet with >48,000 described species and many more undescribed. Parasitoid wasps of this superfamily are mostly beneficial insects that attack and kill other arthropods and are important for understanding diversification and the evolution of life history strategies related to parasitoidism. Further, some lineages of parasitoids within Ichneumonoidea have acquired endogenous virus elements (EVEs) that are permanently a part of the wasp's genome and benefit the wasp through host immune disruption and behavioral control. Unfortunately, understanding the evolution of viral acquisition, parasitism strategies, diversification, and host immune disruption mechanisms, is deeply limited by the lack of a robust phylogenetic framework for Ichneumonoidea. Here we design probes targeting 541 genes across 91 taxa to test phylogenetic relationships, the evolution of parasitoid strategies, and the utility of probes to capture polydnavirus genes across a diverse array of taxa. Phylogenetic relationships among Ichneumonoidea were largely well resolved with most higher-level relationships maximally supported. We noted codon use biases between the outgroups, Braconidae, and Ichneumonidae and within Pimplinae, which were largely solved through analyses of amino acids rather than nucleotide data. These biases may impact phylogenetic reconstruction and caution for outgroup selection is recommended. Ancestral state reconstructions were variable for Braconidae across analyses, but consistent for reconstruction of idiobiosis/koinobiosis in Ichneumonidae. The data suggest many transitions between parasitoid life history traits across the whole superfamily. The two subfamilies within Ichneumonidae that have polydnaviruses are supported as distantly related, providing strong evidence for two independent acquisitions of ichnoviruses. Polydnavirus capture using our designed probes was only partially successful and suggests that more targeted approaches would be needed for this strategy to be effective for surveying taxa for these viral genes. In total, these data provide a robust framework for the evolution of Ichneumonoidea.

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The pollination services provided by bees are essential for supporting natural and agricultural ecosystems. However, bee population declines have been documented across the world. Many of the factors known to undermine bee health (e.g., poor nutrition) can decrease immunocompetence and, thereby, increase bees' susceptibility to diseases. Given the myriad of stressors that can exacerbate disease in wild bee populations, assessments of the relative impact of landscape habitat conditions on bee pathogen prevalence are needed to effectively conserve pollinator populations. Herein, we assess how landscape-level conditions, including various metrics of floral/nesting resources, insecticides, weather, and honey bee (Apis mellifera) abundance, drive variation in wild bumble bee (Bombus impatiens) pathogen loads. Specifically, we screened 890 bumble bee workers from varied habitats in Pennsylvania, USA for three pathogens (deformed wing virus, black queen cell virus, and Vairimorpha (= Nosema) bombi), Defensin expression, and body size. Bumble bees collected within low-quality landscapes exhibited the highest pathogen loads, with spring floral resources and nesting habitat availability serving as the main drivers. We also found higher loads of pathogens where honey bee apiaries are more abundant, a positive relationship between Vairimorpha loads and rainfall, and differences in pathogens by geographic region. Collectively, our results highlight the need to support high-quality landscapes (i.e., those with abundant floral/nesting resources) to maintain healthy wild bee populations.

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While morphological differences such as tongue length are often featured as drivers of pollinator floral preferences, differences in chemical detection and tolerance to secondary compounds may also play a role. We sought to better understand the role of secondary compounds in floral preference by examining visitation of milkweed flowers, which can contain toxic cardenolides in their nectar, by bumble bees (Bombus spp.), some of their most abundant and important pollinators. We examine bumble bee species visitation of common milkweed (Asclepias syriaca) compared to other flowers in the field and test whether observed preferences may be influenced by avoidance and tolerance of cardenolides, as measured by the cardenolide ouabain, in the lab. We reveal that common milkweed is visited predominantly by one bumble bee species, Bombus griseocollis, in a ratio much higher than the abundance of this species in the community. We confirmed the presence and toxicity of cardenolides in A. syriaca nectar. Lab experiments revealed that B. griseocollis, compared to the common bumble bees B. impatiens and B. bimaculatus, exhibit greater avoidance of cardenolides, but only at levels that start to induce illness, whereas the other species exhibit either no or reduced avoidance of cardenolides, resulting in illness and mortality in these bees. Toxicity experiments reveal that B. griseocollis also has a substantially higher tolerance for cardenolides than B. impatiens. Together, these results support a potential evolutionary association between B. griseocollis and milkweed that may involve increased ability to both detect and tolerate milkweed cardenolides.

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Pollinator nutritional ecology provides insights into plant-pollinator interactions, coevolution, and the restoration of declining pollinator populations. Bees obtain their protein and lipid nutrient intake from pollen, which is essential for larval growth and development as well as adult health and reproduction. Our previous research revealed that pollen protein to lipid ratios (P:L) shape bumble bee foraging preferences among pollen host-plant species, and these preferred ratios link to bumble bee colony health and fitness. Yet, we are still in the early stages of integrating data on P:L ratios across plant and bee species. Here, using a standard laboratory protocol, we present over 80 plant species' protein and lipid concentrations and P:L values, and we evaluate the P:L ratios of pollen collected by three bee species. We discuss the general phylogenetic, phenotypic, behavioral, and ecological trends observed in these P:L ratios that may drive plant-pollinator interactions; we also present future research questions to further strengthen the field of pollination nutritional ecology. This dataset provides a foundation for researchers studying the nutritional drivers of plant-pollinator interactions as well as for stakeholders developing planting schemes to best support pollinators.

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Müllerian mimicry theory states that frequency-dependent selection should favour geographical convergence of harmful species onto a shared colour pattern. As such, mimetic patterns are commonly circumscribed into discrete mimicry complexes, each containing a predominant phenotype. Outside a few examples in butterflies, the location of transition zones between mimicry complexes and the factors driving mimicry zones has rarely been examined. To infer the patterns and processes of Müllerian mimicry, we integrate large-scale data on the geographical distribution of colour patterns of social bumblebees across the contiguous United States and use these to quantify colour pattern mimicry using an innovative, unsupervised machine-learning approach based on computer vision. Our data suggest that bumblebees exhibit geographically clustered, but sometimes imperfect colour patterns, and that mimicry patterns gradually transition spatially rather than exhibit discrete boundaries. Additionally, examination of colour pattern transition zones of three comimicking, polymorphic species, where active selection is driving phenotype frequencies, revealed that their transition zones differ in location within a broad region of poor mimicry. Potential factors influencing mimicry transition zone dynamics are discussed.

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