Biology subjects

Grozinger, C. M.

Publications and source records attributed to Grozinger, C. M..

10 recordsLinked to original sources

bioRxiv2024

Intragenomic conflict underlies extreme phenotypic plasticity in queen-worker caste determination in honey bees (Apis mellifera)

Caste determination of honey bees (Apis mellifera) is a prime example of developmental plasticity, where differences in larval diet will result in identical genotypes yielding either long-lived, reproductive queens or short-lived, facultatively sterile workers. Beyond environmental factors, intragenomic conflict between genes inherited from the mother (matrigenes) versus the father (patrigenes) is also hypothesized to generate this plasticity. In honey bees, the Kinship Theory of Intragenomic Conflict predicts selection on patrigenes to enhance traits that result in fitness gained through reproduction, and thus patrigenes should favor the queen caste fate. Here, we conducted allele-specific transcriptome analyses on queen-destined larvae (QL) and worker-destined larvae (WL) at 192 hours post-fertilization (hpf), a critical stage for caste determination. Our findings reveal hundreds of genes with parent-of-origin effects (POEs), with significant patrigene-biased transcription in QL. Genes with POEs in honey bees resemble imprinted genes in other taxa in terms of genomic clustering, recombination rate, intron length and CpG density, and a subset are maintained from 24hpf eggs. Previous studies demonstrated that DNA methylation, the canonical regulatory mechanism underlying transcriptional POEs in placental mammals, angiosperms, and some insects, is not operating in honey bees or other social insects. We use allele-specific ChIP-seq analyses to demonstrate that POEs on caste-specific histone post-translational modification (HPTM) profiles of H3K27me3, H3K4me3 and H3K27ac are associated with POEs on transcription. Together, these findings suggest that parent-of-origin intragenomic conflicts may contribute broadly to phenotypic plasticity and may be associated with HPTMs, suggesting a "non-canonical" genomic imprinting-like system in social insects.

developmental biology↗

bioRxiv2023

Beyond conflict: kinship theory of intragenomic conflict predicts individual variation in altruistic behavior

Studies of the genetic basis of behavioral variation have emphasized gene cooperation within networks, often overlooking gene conflicts. The Kinship Theory of Intragenomic Conflict (KTIC) proposes that conflicts can occur within genes when parent-specific alleles have different strategies for maximizing reproductive fitness. Here, we test a prediction of the KTIC - that selection should favor alleles which promote "altruistic" behaviors that support the reproductive fitness of kin. In honey bee (Apis mellifera) colonies, workers act altruistically when tending to the queen by performing a "retinue" behavior, distributing the queens mandibular pheromone (QMP) throughout the hive. Workers exposed to QMP do not activate their ovaries, ensuring they care for the queens brood instead of competing to lay unfertilized eggs. Thus, the KTIC predicts that response to QMP should be favored by the maternal genome. Using a reciprocal cross design, we tested for parent-of-origin effects on the workers 1) responsiveness to QMP, 2) ovary activation, and 3) brain transcriptome. We hypothesized that QMP-responsive workers have smaller and less active ovaries, influenced by the workers parent-of-origin. With an allele-specific transcriptomic analysis, we tested whether QMP-responsive workers show enriched maternal allele-biased gene expression compared to QMP-unresponsive workers. Finally, we explored how parent-of-origin gene expression patterns are associated with overall gene expression patterns and regulatory networks. We report evidence in support of the KTIC for the retinue behavior and associated conflicts within gene networks. Our study provides new insights into the genetic basis of behavior and the potential for behavioral variation influenced by intragenomic conflict.

animal behavior and cognition↗

bioRxiv2022

Signatures of adaptive decreased virulence of deformed wing virus in an isolated population of wild honey bees (Apis mellifera)

Understanding the ecological and evolutionary processes that drive host-pathogen interactions is critical for combating epidemics and conserving species. The Varroa destructor mite and deformed wing virus (DWV) are two synergistic threats to Western honey bee (Apis mellifera) populations across the globe. Distinct honey bee populations have been found to self-sustain despite Varroa infestations, including colonies within the Arnot Forest outside Ithaca, NY, USA. We hypothesized that in these honey bee populations, DWV has been selected to produce an avirulent infection phenotype, allowing for the persistence of both host and disease-causing agents. To investigate this, we assessed the presence and titer of viruses in bees from the Arnot Forest and managed apiaries, and assessed genomic variation and virulence differences between DWV isolates. Across groups, we found viral abundance was similar, but viral genotypes were distinct. We also found that infections with viral isolates from the Arnot Forest resulted in higher survival and lower rates of symptomatic deformed wings, compared to analogous isolates from managed colonies, providing preliminary evidence to support the hypothesis of adaptive decreased viral virulence. Overall, this multi-level investigation of virus genotype and phenotype across different contexts reveals critical insight into global bee health and the ecological and evolutionary processes that drive host-pathogen interactions.

evolutionary biology↗

bioRxiv2022

Seasonal bee communities vary in their responses local and landscape scales: implication for land managers

ContextThere is great interest in land management practices for pollinators; however, a quantitative comparison of landscape and local effects on bee communities is necessary to determine if adding small habitat patches can increase bee abundance or species richness. The value of increasing floral abundance at a site is undoubtedly influenced by the phenology and magnitude of floral resources in the landscape, but due to the complexity of measuring landscape-scale resources, these factors have been understudied. ObjectivesTo address this knowledge gap, we quantified the relative importance of local versus landscape scale resources for bee communities, identified the most important metrics of local and landscape quality, and evaluated how these relationships vary with season. MethodsWe studied season-specific relationships between local and landscape quality and wild-bee communities at 33 sites in the Finger Lakes region of New York, USA. We paired site surveys of wild bees, plants, and soil characteristics with a multi-dimensional assessment of landscape composition, configuration, insecticide toxic load, and a spatio-temporal evaluation of floral resources at local and landscape scales. ResultsWe found that the most relevant spatial scale varied by season. Spring bees depended on landscape resources, but summer bees responded more to local quality, implying that site-level management is most likely to be successful in supporting summer bees. Semi-natural habitats, including forests, wetlands, and other aquatic habitats, were particularly important for spring bees. ConclusionsBy considering spatial and temporal variation in resources, we developed season-specific recommendations to improve habitat quality for wild bees and offset manifold stressors threatening these essential pollinators.

ecology↗

bioRxiv2021

Putting pesticides on the map for pollinator research and conservation

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 in the contiguous United States, we describe a method to map pesticide indicators at spatial scales relevant to pollinator research and conservation.

ecology↗

bioRxiv2019

Characterizing the floral resources of a North American metropolis using a honey bee foraging assay

Roughly a third of described insect species visit flowers, making the flower-insect interface one of the chief pillars of global biodiversity. Studying flower-insect relationships at the scale of communities and landscapes has been hindered, however, by the methodological challenges of quantifying landscape-scale floral resources. This challenge is especially acute in urban landscapes, where traditional floral surveying techniques are ill-suited to the unique constraints of built environments. To surmount these challenges, we devised a \"honey bee foraging assay\" approach to floral resource surveying, wherein continuous colony weight tracking and DNA metabarcoding of pollen samples are used to capture both the overall availability and taxonomic composition of floral resources. We deploy this methodology in the complex urban ecosystem of Philadelphia, PA, U.S. Our results reveal distinct seasonality of floral resource availability, with pulses of high availability in May, June, and September, and a period of prolonged scarcity in August. Pollen genus richness mirrored this pattern, with peak richness in May and June. The taxonomic composition of pollen samples varied seasonally, reflecting underlying floral phenology, with especially strong turnover between May and June samples and between August and September samples delineating well-defined spring, summer, and fall floral resource communities. Trait analysis also revealed marked seasonal structure, with spring samples characterized by trees and shrubs, summer samples including a stronger presence of herbaceous \"weeds\", and fall samples dominated by woody vines. Native flora predominated in spring, giving way to a preponderance of exotic flora in summer and fall. Our study provides a detailed portrait of floral resources in a complex urban environment. At a basic level, this yields insight into the assembly of novel urban floral resource communities, showcasing, for example, the emergence of a woody-vine-dominated fall flora. At an applied level, our data can inform urban land management, such as the design of ecologically functional ornamental plantings, while also providing practical guidance to beekeepers seeking to adapt their management activities to floral resource seasonality. Methodologically, our study demonstrates the potential of the honey bee foraging assay as an efficient and standardizable technique for landscape-scale floral resource surveying.

ecology↗

bioRxiv2019

Rising insecticide potency outweighs falling application rate to make US farmland increasingly hazardous to insects

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 insect decline. Nevertheless, answers to basic questions about the spatiotemporal patterns of insecticide use remain elusive, due in part to the inherent complexity of insecticide use, and exacerbated by the dispersed nature of the relevant data, divided between several government repositories. Here, we integrate these public datasets to generate county-level annual estimates of total insect 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 drivers of the observed changes, we divide insect toxic load into the components of extent (area treated) and intensity (application rate x potency). We show that while contact-based insect toxic load remained relatively steady over the period of our analysis, oral-based insect toxic load increased roughly 9-fold, with reductions in application rate outweighed by disproportionate increases in potency (toxicity/kg) and increases in extent. This pattern varied markedly by region, with the greatest increases seen in Heartland and Northern Great Plains regions, likely driven by use of neonicotinoid seed treatments in corn and soybean. In this \"potency paradox,\" US farmland has become more hazardous to insects despite lower volumes of insecticides applied, raising serious concerns about insect conservation and highlighting the importance of integrative approaches to pesticide use monitoring.\n\nSignificance statementPrevious analyses disagree about whether US insecticide use is increasing or decreasing, a question of significant importance given the putative role of insecticides in recent insect declines. We integrated information from multiple national databases to estimate insect toxic load (represented as honey bee lethal doses) of the agricultural insecticides applied in each US county from 1997 to 2012, and factors responsible for its change. Across the US, insect toxic load - calculated on the basis of oral toxicity - increased 9-fold. This increase was due to increases in the potency (toxicity/kg) of insecticides applied and in the area treated; the volume of insecticides applied declined. Toxic load increased most dramatically in regions where neonicotinoid seed treatments for field crops are commonly used.

ecology↗

bioRxiv2019

Honey bee (Apis mellifera) larval pheromones regulate gene expression related to foraging task specialization

BackgroundForaging behavior in honey bees (Apis mellifera) is a complex phenotype which is regulated by physiological state and social signals. How these factors are integrated at the molecular level to modulate foraging behavior has not been well-characterized. The transition of worker bees from nursing to foraging behavior is mediated by large-scale changes in brain gene expression, which are influenced by pheromones produced by the queen and larvae. Larval pheromones can also stimulate foragers to leave the colony to collect pollen, but the mechanisms underpinning this rapid behavioral plasticity are unknown. Furthermore, the mechanisms through which foragers specialize on collecting nectar or pollen, and how larval pheromones impact these different behavioral states, remains to be determined. Here, we investigated the patterns of gene expression related to rapid behavioral plasticity and task allocation among honey bee foragers exposed to two larval pheromones, brood pheromone (BP) and (E)-beta-ocimene (EBO).\n\nResultsWe hypothesized that both pheromones would alter expression of genes in the brain related to foraging and would differentially impact expression of genes in the brains of pollen compared to nectar foragers. Combining data reduction, clustering, and network analysis methods, we found that foraging preference (nectar vs. pollen) and pheromone exposure are each associated with specific brain gene expression profiles. Furthermore, pheromone exposure has a strong transcriptional effect on genes that are preferentially expressed in nectar foragers. Representation factor analysis between our study and previous landmark honey bee transcriptome studies revealed significant overlaps for both pheromone communication and foraging task specialization.\n\nConclusionsSocial signals (i.e. pheromones) may invoke foraging-related genes to upregulate pollen foraging at both long and short time scales. These results provide new insights into how social signals integrate with task specialization at the molecular level and highlights the important role that brain gene expression plays in behavioral plasticity across time scales.

genomics↗

bioRxiv2018

Haemolymph removal by the parasite Varroa destructor can trigger the proliferation of the Deformed Wing Virus in mite infested bees (Apis mellifera), contributing to enhanced pathogen virulence

The association between the Deformed Wing Virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honey bee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, in particular, the causes of viral proliferation in mite infested bees.\n\nHere we develop and test a novel hypothesis - grounded in ecological predator-prey theory - that mite feeding destabilizes viral immune control through the removal of both viral prey and immune predators, triggering uncontrolled viral replication. Consistent with this hypothesis, we show that experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. In contrast, we find no support for alternative proposed mechanisms of viral expansion via mite immune-suppression or within-host viral evolution.\n\nOverall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honey bee health decline and colony losses.

ecology↗

bioRxiv2018

Investigating the viral ecology of global bee communities with high-throughput metagenomics

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate the impacts of other environmental stressors, and, importantly, are readily shared across multiple bee species in a community. However, our understanding of bee viral communities is limited, as it is primarily derived from studies of North American and European Apis mellifera populations. Here, we examined viruses in populations of A. mellifera and 11 other bee species from 9 countries, across 5 continents and Oceania. We developed a novel pipeline to rapidly, inexpensively, and robustly screen for bee viruses. This pipeline includes purification of encapsulated RNA/DNA viruses, sequence-independent amplification, high throughput sequencing, integrated assembly of contigs, and filtering to identify contigs specifically corresponding to viral sequences. We identified sequences corresponding to (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 29 represented by >0.1 % of the reads in a given sample. These viruses and viral families were distributed across multiple regions and species. This study provides a robust pipeline for metagenomics analysis of viruses, and greatly expands our understanding of the diversity of viruses found in bee communities.

genomics↗