@misc{tarpy_2024, title={Collective decision-making during reproduction in social insects: a conceptual model for queen supersedure in honey bees (Apis mellifera)}, volume={66}, ISSN={["2214-5753"]}, DOI={10.1016/j.cois.2024.101260}, abstractNote={Insect societies have served as excellent examples for co-ordinated decision-making. The production of sexuals is the most important group decision that social insects face since it affects both direct and indirect fitness. The behavioral processes by which queens are selected have been of particular interest since they are the primary egg layers that enable colony function. As a model system, previous research on honey bee reproduction has focused on swarming behavior and nest site selection. One significant gap in our knowledge of the collective decision-making process over reproduction is how daughter queens simply replace old or failing queens (=supersedure) rather than being reared for the purposes of colony fission (=swarming) or queen loss (=emergency queen rearing). Here, I present a conceptual model that provides a framework for understanding the collective decisions by colonies to supersede their mother queens, as well as provide some key recommendations on future empirical work.}, journal={CURRENT OPINION IN INSECT SCIENCE}, author={Tarpy, David R.}, year={2024}, month={Dec} }
@article{chapman_mcafee_tarpy_fine_rempel_peters_currie_foster_2024, title={Common viral infections inhibit egg laying in honey bee queens and are linked to premature supersedure}, volume={14}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-024-66286-5}, abstractNote={With their long lives and extreme reproductive output, social insect queens have escaped the classic trade-off between fecundity and lifespan, but evidence for a trade-off between fecundity and immunity has been inconclusive. This is in part because pathogenic effects are seldom decoupled from effects of immune induction. We conducted parallel, blind virus infection experiments in the laboratory and in the field to interrogate the idea of a reproductive immunity trade-off in honey bee (Apis mellifera) queens and to better understand how these ubiquitous stressors affect honey bee queen health. We found that queens injected with infectious virus had smaller ovaries and were less likely to recommence egg-laying than controls, while queens injected with UV-inactivated virus displayed an intermediate phenotype. In the field, heavily infected queens had smaller ovaries and infection was a meaningful predictor of whether supersedure cells were observed in the colony. Immune responses in queens receiving live virus were similar to queens receiving inactivated virus, and several of the same immune proteins were negatively associated with ovary mass in the field. This work supports the hypothesized relationship between virus infection and symptoms associated with queen failure and suggests that a reproductive-immunity trade-off is partially, but not wholly responsible for these effects.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Chapman, Abigail and McAfee, Alison and Tarpy, David R. and Fine, Julia and Rempel, Zoe and Peters, Kira and Currie, Rob and Foster, Leonard J.}, year={2024}, month={Jul} }
@article{levenson_metz_tarpy_2024, title={Effects of study design parameters on estimates of bee abundance and richness in agroecosystems: a meta-analysis}, volume={1}, ISSN={["1938-2901"]}, url={https://doi.org/10.1093/aesa/saae001}, DOI={10.1093/aesa/saae001}, abstractNote={Abstract
Pollinators are critical for agricultural production and food security, leading to many ongoing surveys of pollinators (especially bees) in crop and adjacent landscapes. These surveys have become increasingly important to better understand the community of potential pollinators, quantify relative insect abundance, and secure crop ecosystem services. However, as some bee populations are declining, there is a need to align and improve bee survey efforts, so that they can best meet research and conservation goals, particularly in light of the logistical and financial constraints of conducting such studies. Here, we mined the existing literature on bee surveys in or around agricultural lands to better understand how sampling methods can be optimized to maximize estimates of 2 key measures of bee communities (abundance and richness). After reviewing 72 papers spanning 20 yr of publication, we found that study duration, number of sites, sampling time, and sampling method most significantly influenced abundance, while the number of trips per year and collection method significantly influenced richness. Our analysis helps to derive thresholds, priorities, and recommendations that can be applied to future studies describing bee communities in agroecosystems.}, journal={ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA}, author={Levenson, Hannah K. and Metz, Bradley N. and Tarpy, David R.}, editor={Parys, KatherineEditor}, year={2024}, month={Jan} }
@article{mcafee_chapman_bao_tarpy_foster_2024, title={Investigating trade-offs between ovary activation and immune protein expression in bumble bee (Bombus impatiens) workers and queens}, volume={291}, ISSN={["1471-2954"]}, DOI={10.1098/rspb.2023.2463}, abstractNote={
Evidence for a trade-off between reproduction and immunity has manifested in many animal species, including social insects. However, investigations in social insect queens present a conundrum: new gynes of many social hymenopterans, such as bumble bees and ants, must first mate, then transition from being solitary to social as they establish their nests, thus experiencing confounding shifts in environmental conditions. Worker bumble bees offer an opportunity to investigate patterns of immune protein expression associated with ovary activation while minimizing extraneous environmental factors and genetic differences. Here, we use proteomics to interrogate the patterns of immune protein expression of female bumble bees (
Bombus impatiens
) by (i) sampling queens at different stages of their life cycle, then (ii) by sampling workers with different degrees of ovary activation. Patterns of immune protein expression in the haemolymph of queens are consistent with a reproduction–immunity trade-off, but equivalent samples from workers are not. This brings into question whether queen bumble bees really experience a reproduction–immunity trade-off, or if patterns of immune protein expression may actually be due to the selective pressure of the different environmental conditions they are exposed to during their life cycle.
}, number={2015}, journal={PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES}, author={Mcafee, Alison and Chapman, Abigail and Bao, Grace and Tarpy, David R. and Foster, Leonard J.}, year={2024}, month={Jan} }
@article{caesar_rice_mcafee_underwood_ganote_tarpy_foster_newton_klassen_2024, title={Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages}, volume={1}, ISSN={["2379-5077"]}, DOI={10.1128/msystems.01182-23}, abstractNote={
The queen caste plays a central role in colony success in eusocial insects, as queens lay eggs and regulate colony behavior and development. Queen failure can cause colonies to collapse, which is one of the major concerns of beekeepers. Thus, understanding the biology behind the queen’s health is a pressing issue. Previous studies have shown that the bee microbiome plays an important role in worker bee health, but little is known about the queen microbiome and its function
in vivo
. Here, we characterized the queen microbiome, identifying for the first time the present species and their putative functions. We show that the queen microbiome has predicted nutritional and protective roles in queen association and comprises only four consistently present bacterial species. Additionally, we bring to attention the spread of phages in the queen microbiome, which increased in abundance in failing queens and may impact the fate of the colony.
}, journal={MSYSTEMS}, author={Caesar, Lilian and Rice, Danny W. and Mcafee, Alison and Underwood, Robyn and Ganote, Carrie and Tarpy, David R. and Foster, Leonard J. and Newton, Irene L. G. and Klassen, Jonathan L.}, year={2024}, month={Jan} }
@article{metz_molina-marciales_strand_rueppell_tarpy_amiri_2024, title={Physiological trade-offs in male social insects: Interactions among infection, immunity, fertility, size, and age in honey bee drones}, volume={159}, ISSN={["1879-1611"]}, DOI={10.1016/j.jinsphys.2024.104720}, abstractNote={Female social insects represent a dramatic exception of the evolutionarily conserved physiological trade-off between reproduction and life span, where aging is positively correlated with reproduction. However, whether this facet of life history also pertains to male social insects, remains largely unknown. Male honey bees (drones) die in the act of copulation, placing them under opposing selective pressures. At the individual level, there is inter-male competition for a single successful mating attempt, leading to selective pressure that favors an increase in male fitness. Honey bee drones are haploid individuals and lack the allelic variation in their genome compared to diploid females. We hypothesized that this genetic limitation may result in trade-offs between pathological stress and fitness traits in honey bee males. In our study, we observed differences in size and fertility measures in old and young drones along with stressors of several endemic viruses and the transcriptional immune response. We found that infection does not appear to decrease fertility in old drones, despite evidence for a shift in immune expression away from established mechanisms. Contrary to our expectations, drones additionally do not appear to exhibit a physiological trade-off between size and fertility. These findings demonstrate that drones of different size are likely of different mating quality and that higher quality drones likely favor retaining reproductive output over immune function.}, journal={JOURNAL OF INSECT PHYSIOLOGY}, author={Metz, Bradley N. and Molina-Marciales, Tatiana and Strand, Micheline K. and Rueppell, Olav and Tarpy, David R. and Amiri, Esmaeil}, year={2024}, month={Dec} }
@article{han_amiri_wei_tarpy_strand_xu_rueppell_2023, title={Group size influences maternal provisioning and compensatory larval growth in honeybees}, volume={26}, ISSN={["2589-0042"]}, DOI={10.1016/j.isci.2023.108546}, abstractNote={Environmental variation selects for the adaptive plasticity of maternal provisioning. Even though developing honeybees find themselves in a protected colony environment, their reproductively specialized queens actively adjust their maternal investment, even among worker-destined eggs. However, the potentially adaptive consequences of this flexible provisioning strategy and their mechanistic basis are unknown. Under natural conditions, we find that the body size of larvae hatching from small eggs in large colonies converges with that of initially larger larvae hatching from large eggs typically produced in small colonies. However, large eggs confer a persistent body size advantage when small and large eggs are cross-fostered in small and large colonies, respectively. We substantiate the increased maternal investment by identifying growth-promoting metabolomes and proteomes in large eggs compared to small eggs, which are primarily enriched in amino acid metabolism and cell maturation. Thus, our study provides a comprehensive adaptive explanation for the worker egg size plasticity of honeybees.}, number={12}, journal={ISCIENCE}, author={Han, Bin and Amiri, Esmaeil and Wei, Qiaohong and Tarpy, David R. and Strand, Micheline K. and Xu, Shufa and Rueppell, Olav}, year={2023}, month={Dec} }
@article{tarpy_caren_delaney_2023, title={Meta-analysis of genetic diversity and intercolony relatedness among reproductives in commercial honey bee populations}, volume={3}, ISSN={["2673-8600"]}, DOI={10.3389/finsc.2023.1112898}, abstractNote={Honey bee colonies are large kin groups, each with a single mother queen and thousands of female workers. Queen bees are highly polyandrous, each mating with an average of approximately 12 drones from other colonies. We used a meta-analysis approach to compare the pedigree relationships of honey bee reproductives (queens and their mates) across five different studies and to quantify the overall genetic diversity of breeding populations. We compared the inferred genotypes of queens and their mates from microsatellite analyses of worker offspring from a feral Africanized honey bee population (which served as a negative control for inbreeding), an experimentally derived population of sister queens (which served as a positive control for inbreeding), and three separate commercially managed populations. We then compared the relatedness of all drones mated to each queen (mate-mate), all queens within each population (queen-queen), each queen with each of her mates (queen-mate), and all drones within each population (drone-drone). We found, as expected, the lowest levels of genetic similarity in the outcrossed population and highest levels of genetic similarity in the inbred population. Levels of genetic similarity among the managed honey bee populations were intermediate but closer to that of the inbred population. Genetic structuring of the entire breeding population resulted in two major subpopulations, likely deriving from breeders on the east and west coast. The effects that these findings have on the overall population genetic diversity of managed honey bees is discussed.}, journal={FRONTIERS IN INSECT SCIENCE}, author={Tarpy, David R. and Caren, Joel R. and Delaney, Deborah A.}, year={2023}, month={Jan} }
@article{mcafee_metz_milone_foster_tarpy_2022, title={Drone honey bees are disproportionately sensitive to abiotic stressors despite expressing high levels of stress response proteins}, volume={5}, ISSN={["2399-3642"]}, DOI={10.1038/s42003-022-03092-7}, abstractNote={AbstractDrone honey bees (Apis mellifera) are the obligate sexual partners of queens, and the availability of healthy, high-quality drones directly affects a queen’s fertility and productivity. Yet, our understanding of how stressors affect adult drone fertility, survival, and physiology is presently limited. Here, we investigated sex biases in susceptibility to abiotic stressors (cold stress, topical imidacloprid exposure, and topical exposure to a realistic cocktail of pesticides). We found that drones (haploid males) were more sensitive to cold and imidacloprid exposure than workers (sterile, diploid females), but the cocktail was not toxic at the concentrations tested. We corroborated this lack of cocktail toxicity with in-hive exposures via pollen feeding. We then used quantitative proteomics to investigate protein expression profiles in the hemolymph of topically exposed workers and drones, and found that 34 proteins were differentially expressed in exposed drones relative to controls, but none were differentially expressed in exposed workers. Contrary to our hypothesis, we show that drones express surprisingly high baseline levels of putative stress response proteins relative to workers. This suggests that drones’ stress tolerance systems are fundamentally rewired relative to workers, and susceptibility to stress depends on more than simply gene dose or allelic diversity.}, number={1}, journal={COMMUNICATIONS BIOLOGY}, author={McAfee, Alison and Metz, Bradley N. and Milone, Joseph P. and Foster, Leonard J. and Tarpy, David R.}, year={2022}, month={Feb} }
@article{levenson_tarpy_2022, title={Effects of planted pollinator habitat on pathogen prevalence and interspecific detection between bee species}, volume={12}, ISSN={["2045-2322"]}, url={https://doi.org/10.1038/s41598-022-11734-3}, DOI={10.1038/s41598-022-11734-3}, abstractNote={AbstractShared resources can instigate pathogen spread due to large congregations of individuals in both natural and human modified resources. Of current concern is the addition of pollinator habitat in conservation efforts as it attracts bees of various species, potentially instigating interspecific sharing of pathogens. Common pathogens have been documented across a wide variety of pollinators with shared floral resources instigating their spread in some, but not all, cases. To evaluate the impact of augmented pollinator habitat on pathogen prevalence, we extracted RNA from samples of eight bee species across three families and screened these samples for nine pathogens using RT-qPCR. We found that some habitat characteristics influenced pathogen detection; however, we found no evidence that pathogen detection in one bee species was correlated with pathogen detection in another. In fact, pathogen detection was rare in wild bees. While gut parasites were detected in 6 out of the 8 species included in this study, viruses were only detected in honey bees. Further, virus detection in honey bees was low with a maximum 21% of samples testing positive for BQCV, for example. These findings suggest factors other than the habitat itself may be more critical in the dissemination of pathogens among bee species. However, we found high relative prevalence and copy number of gut parasites in some bee species which may be of concern, such asBombus pensylvanicus. Long-term monitoring of pathogens in different bee species at augmented pollinator habitat is needed to evaluate if these patterns will change over time.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Levenson, Hannah K. and Tarpy, David R.}, year={2022}, month={May} }
@article{levenson_sharp_tarpy_2022, title={Evaluating the impact of increased pollinator habitat on bee visitation and yield metrics in soybean crops}, volume={331}, ISSN={["1873-2305"]}, url={http://dx.doi.org/10.1016/j.agee.2022.107901}, DOI={10.1016/j.agee.2022.107901}, abstractNote={Agricultural intensification has significantly altered ecosystem functioning and aided in the reduction of global biodiversity. While agriculture requires increased reliance on animal pollination, pollinator populations have declined. To combat this, adding pollinator habitat into agricultural landscapes is increasingly common, but many questions remain about its functionality and impact on agroecosystems, particularly in pollinator-independent crops. Our study uses pollinator habitats planted on experimental research stations in the southeastern USA to evaluate their impact on pollinator communities within a nearby cropping system (soybeans) and the resulting yield. We found the species composition of pollinator communities within the habitat to be significantly different than the communities in soybeans. Even still, we identified more than 30 bee species visiting soybean flowers and verified that a subset of these species had actively collected soybean pollen. Bees from soybean fields planted adjacent to the habitat had more habitat pollen types present, while some species had more non-habitat types present when in the negative control sites. The presence of habitat had a positive effect on some yield measurements with adjacent soybean sites having 6.52% heavier seeds per plant on average. These findings demonstrate that pollinator habitat can be an important resource for supporting pollinators and highlights the importance of considering pollinator habitat in pollinator-independent crops, as they may still benefit from and be attractive to pollinator communities. • We investigated effects of pollinator habitat in a putative pollinator-independent crop. • Bee communities differ between soybean fields and pollinator habitat. • Bees visiting soybean flowers collected soybean pollen. • Bees in soybean fields far from pollinator habitat gathered more environmental pollen. • Seed weight increased in soybean fields planted near pollinator habitat.}, journal={AGRICULTURE ECOSYSTEMS & ENVIRONMENT}, publisher={Elsevier BV}, author={Levenson, Hannah K. and Sharp, April E. and Tarpy, David R.}, year={2022}, month={Jun} }
@article{chapman_amiri_han_mcdermott_rueppell_tarpy_foster_mcafee_2022, title={Fertility costs of cryptic viral infections in a model social insect}, volume={12}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-022-20330-4}, abstractNote={AbstractDeclining insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Here, we investigated viruses as a threat to social insect reproduction, using honey bees as a model species. We report that in two independent surveys (N = 93 and N = 54, respectively) of honey bee (Apis mellifera) queens taken from a total of ten beekeeping operations across British Columbia, high levels of natural viral infection are associated with decreased ovary mass. Failed (poor quality) queens displayed higher levels of viral infection, reduced sperm viability, smaller ovaries, and altered ovary protein composition compared to healthy queens. We experimentally infected queens with Israeli acute paralysis virus (IAPV) and found that the ovary masses of IAPV-injected queens were significantly smaller than control queens, demonstrating a causal relationship between viral infection and ovary size. Queens injected with IAPV also had significantly lower expression of vitellogenin, the main source of nutrition deposited into developing oocytes, and higher levels of heat-shock proteins, which are part of the honey bee’s antiviral response. This work together shows that viral infections occurring naturally in the field are compromising queen reproductive success.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Chapman, Abigail and Amiri, Esmaeil and Han, Bin and McDermott, Erin and Rueppell, Olav and Tarpy, David R. and Foster, Leonard J. and McAfee, Alison}, year={2022}, month={Sep} }
@article{simone-finstrom_strand_tarpy_rueppell_2022, title={Impact of Honey Bee Migratory Management on Pathogen Loads and Immune Gene Expression is Affected by Complex Interactions With Environment, Worker Life History, and Season}, volume={22}, ISSN={["1536-2442"]}, DOI={10.1093/jisesa/ieab096}, abstractNote={AbstractThe effects of honey bee management, such as intensive migratory beekeeping, are part of the ongoing debate concerning causes of colony health problems. Even though comparisons of disease and pathogen loads among differently managed colonies indicate some effects, the direct impact of migratory practices on honey bee pathogens is poorly understood. To test long- and short-term impacts of managed migration on pathogen loads and immunity, experimental honey bee colonies were maintained with or without migratory movement. Individuals that experienced migration as juveniles (e.g., larval and pupal development), as adults, or both were compared to control colonies that remained stationary and therefore did not experience migratory relocation. Samples at different ages and life-history stages (hive bees or foragers), taken at the beginning and end of the active season, were analyzed for pathogen loads and physiological markers of health. Bees exposed to migratory management during adulthood had increased levels of the AKI virus complex (Acute bee paralysis, Kashmir bee, and Israeli acute bee paralysis viruses) and decreased levels of antiviral gene expression (dicer-like). However, those in stationary management as adults had elevated gut parasites (i.e. trypanosomes). Effects of environment during juvenile development were more complex and interacted with life-history stage and season. Age at collection, life-history stage, and season all influenced numerous factors from viral load to immune gene expression. Although the factors that we examined are not independent, the results illuminate potential factors in both migratory and nonmigratory beekeeping that are likely to contribute to colony stress, and also indicate potential mitigation measures.}, number={1}, journal={JOURNAL OF INSECT SCIENCE}, author={Simone-Finstrom, Michael and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2022}, month={Jan} }
@article{han_wei_amiri_hu_meng_strand_tarpy_xu_li_rueppell_2022, title={The molecular basis of socially induced egg-size plasticity in honey bees}, volume={11}, ISSN={["2050-084X"]}, DOI={10.7554/eLife.80499}, abstractNote={Reproduction involves the investment of resources into offspring. Although variation in reproductive effort often affects the number of offspring, adjustments of propagule size are also found in numerous species, including the Western honey bee, Apis mellifera. However, the proximate causes of these adjustments are insufficiently understood, especially in oviparous species with complex social organization in which adaptive evolution is shaped by kin selection. Here, we show in a series of experiments that queens predictably and reversibly increase egg size in small colonies and decrease egg size in large colonies, while their ovary size changes in the opposite direction. Additional results suggest that these effects cannot be solely explained by egg-laying rate and are due to the queens’ perception of colony size. Egg-size plasticity is associated with quantitative changes of 290 ovarian proteins, most of which relate to energy metabolism, protein transport, and cytoskeleton. Based on functional and network analyses, we further study the small GTPase Rho1 as a candidate regulator of egg size. Spatio-temporal expression analysis via RNAscope and qPCR supports an important role of Rho1 in egg-size determination, and subsequent RNAi-mediated gene knockdown confirmed that Rho1 has a major effect on egg size in honey bees. These results elucidate how the social environment of the honey bee colony may be translated into a specific cellular process to adjust maternal investment into eggs. It remains to be studied how widespread this mechanism is and whether it has consequences for population dynamics and epigenetic influences on offspring phenotype in honey bees and other species.}, journal={ELIFE}, author={Han, Bin and Wei, Qiaohong and Amiri, Esmaeil and Hu, Han and Meng, Lifeng and Strand, Micheline K. and Tarpy, David R. and Xu, Shufa and Li, Jianke and Rueppell, Olav}, year={2022}, month={Nov} }
@article{metz_tarpy_2022, title={Variation in the reproductive quality of honey bee males affects their age of flight attempt}, volume={10}, ISSN={["2167-8359"]}, DOI={10.7717/peerj.13859}, abstractNote={
Background
Honey bee males (drones) exhibit life histories that enable a high potential for pre- or post-copulatory sperm competition. With a numerical sex ratio of ∼11,000 drones for every queen, they patrol flyways and congregate aerially to mate on the wing. However, colonies and in fact drones themselves may benefit from a relative lack of competition, as queens are highly polyandrous, and colonies have an adaptive advantage when headed by queens that are multiply mated. Previous research has shown that larger drones are more likely to be found at drone congregation areas, more likely to mate successfully, and obtain a higher paternity share. However, the reproductive quality and size of drones varies widely within and among colonies, suggesting adaptive maintenance of drone quality variation at different levels of selection.
Methods
We collected drones from six colony sources over the course of five days. We paint marked and individually tagged drones after taking body measurements at emergence and then placed the drones in one of two foster colonies. Using an entrance cage, we collected drones daily as they attempted flight. We collected 2,420 drones live or dead, analyzed 1,891 for attempted flight, collected emergence data on 207 drones, and dissected 565 upon capture to assess reproductive maturity. We measured drone body mass, head width, and thorax width at emergence, and upon dissection we further measured thorax mass, seminal vesicle length, mucus gland length, sperm count, and sperm viability from the seminal vesicles.
Results
We found that drones that were more massive at emergence were larger and more fecund upon capture, suggesting that they are of higher reproductive quality and therefore do not exhibit a trade-off between size and fecundity. However, smaller drones tended to attempt initial flight at a younger age, which suggests a size trade-off not with fecundity but rather developmental maturation. We conclude that smaller drones may take more mating flights, each individually with a lower chance of success but thereby increasing their overall fitness. In doing so, the temporal spread of mating attempts of a single generation of drones within a given colony increases colony-level chances of mating with nearby queens, suggesting an adaptive rationale for high variation among drone reproductive quality within colonies.
}, journal={PEERJ}, author={Metz, Bradley N. and Tarpy, David R.}, year={2022}, month={Aug} }
@article{swami_ganser_tarpy_strand_li-byarlay_2021, title={Assessment and Comparison of Two Different Methods to Extract Nucleic Acids From Individual Honey Bees}, volume={114}, ISSN={["1938-2901"]}, DOI={10.1093/aesa/saab027}, abstractNote={AbstractThe honey bee is an excellent model system to study behavioral ecology, behavioral genetics, and sociogenomics. Nucleic acid-based analyses enable a broad scope of research in functional genomics, disease diagnostics, mutant screening, and genetic breeding. Multiple levels of analysis lead to a more comprehensive understanding of the causes of phenotypic variation by integrating genomic variation, transcriptomic profiles, and epigenomic information. One limitation, however, is the sample preparation procedures to obtain high quality DNA and RNA simultaneously, particularly from small amounts of material, such as tissues of individual bees. We demonstrate that it is feasible to perform dual extractions of DNA and RNA from a single individual bee and compare the quality and quantity of the extracted nucleic acids using two different types of methods. There was a greater total yield of DNA and RNA from ethanol-based extractions with minimal differences in overall concentration in ng/uL. We describe here the first validated method for dual extraction of DNA and RNA specifically from individual honey bees (Apis mellifera).}, number={5}, journal={ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA}, author={Swami, Rohan and Ganser, Brooke and Tarpy, David R. and Strand, Micheline K. and Li-Byarlay, Hongmei}, year={2021}, month={Sep}, pages={614–619} }
@article{mcafee_milone_metz_mcdermott_foster_tarpy_2021, title={Honey bee queen health is unaffected by contact exposure to pesticides commonly found in beeswax}, volume={11}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-021-94554-1}, abstractNote={AbstractHoney bee queen health is crucial for colony health and productivity, and pesticides have been previously associated with queen loss and premature supersedure. Prior research has investigated the effects of indirect pesticide exposure on queens via workers, as well as direct effects on queens during development. However, as adults, queens are in constant contact with wax as they walk on comb and lay eggs; therefore, direct pesticide contact with adult queens is a relevant but seldom investigated exposure route. Here, we conducted laboratory and field experiments to investigate the impacts of topical pesticide exposure on adult queens. We tested six pesticides commonly found in wax: coumaphos, tau-fluvalinate, atrazine, 2,4-DMPF, chlorpyriphos, chlorothalonil, and a cocktail of all six, each administered at 1, 4, 8, 16, and 32 times the concentrations typically found in wax. We found no effect of any treatment on queen mass, sperm viability, or fat body protein expression. In a field trial testing queen topical exposure of a pesticide cocktail, we found no impact on egg-laying pattern, queen mass, emergence mass of daughter workers, and no proteins in the spermathecal fluid were differentially expressed. These experiments consistently show that pesticides commonly found in wax have no direct impact on queen performance, reproduction, or quality metrics at the doses tested. We suggest that previously reported associations between high levels of pesticide residues in wax and queen failure are most likely driven by indirect effects of worker exposure (either through wax or other hive products) on queen care or queen perception.}, number={1}, journal={SCIENTIFIC REPORTS}, author={McAfee, Alison and Milone, Joseph P. and Metz, Bradley and McDermott, Erin and Foster, Leonard J. and Tarpy, David R.}, year={2021}, month={Jul} }
@article{tarpy_talley_metz_2020, title={Influence of brood pheromone on honey bee colony establishment and queen replacement}, volume={60}, ISSN={["2078-6913"]}, DOI={10.1080/00218839.2020.1867336}, abstractNote={There is both anecdotal and empirical evidence to suggest that honey bee queen longevity has decreased in recent years, leading to premature supersedure and queen failure. This is particularly evident when beekeepers create new colonies from packages, where many queens are immediately rejected or replaced after only a few weeks. Relatively little is known about the mechanisms that trigger supersedure in honey bees, although previous studies have shown a strong link with open brood suggesting that brood ester pheromone (BEP) may be involved. We installed new packages into hive equipment with either no treatment (Control), exposure to BEP during package transport and for the first 10 days after installation (BEP), or one frame of open brood (Brood). We found that over the course of the 12-week experiment, Control colonies grew the least, Brood colonies started stronger but leveled off similar to Control colonies, and BEP colonies grew slowly initially but continued positive growth through the end of the experiment. Moreover, we found a highly significant effect of treatment on Outcome—whether the initial queens were immediately Rejected (within 5 weeks), Superseded (after 5 weeks), or Accepted, with Brood, BEP, and Control colonies having 86.7%, 53.3%, and 33.3% acceptance, respectively. Finally, we found that the open-brood:adult-bees ratio significantly diverged 3 weeks prior to queen replacement between accepting and replacing colonies. We suggest that while BEP alone is insufficient to deter premature supersedure, there are clear benefits to queen longevity and package-installation success when establishing new colonies with frames of young brood.}, number={2}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Tarpy, David R. and Talley, Eric and Metz, Bradley N.}, year={2020}, month={Dec}, pages={220–228} }
@article{rusert_pettis_tarpy_2021, title={Introduction of Varroa destructor has not altered honey bee queen mating success in the Hawaiian archipelago}, volume={11}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-020-80525-5}, abstractNote={AbstractBeekeepers struggle to minimize the mortality of their colonies as a consequence of the parasitic mite Varroa destructor in order to maintain a sustainable managed pollinator population. However, little is known about how varroa mites might diminish local populations of honey bee males (drones) that might affect the mating success of queens. As one of the world’s last localities invaded by varroa mites, the Hawaiian Islands offer a unique opportunity to examine this question by comparing queens mated on mite-infested and mite-free islands. We raised queen bees on four Hawaiian Islands (Kaua‘i, O‘ahu, Maui, and Hawai‘i) and subsequently collected their offspring to determine queen mating frequency and insemination success. No significant difference for mating success was found between the islands with and without varroa mites, and relatively high levels of polyandry was detected overall. We also found a significant association between the number of sperm stored in the queens’ spermathecae and the number of managed colonies within the localities of the queens mated. Our findings suggest that varroa mites, as they currently occur in Hawai‘i, may not significantly reduce mating success of honey bee queens, which provides insight for both the reproductive biology of honey bees as well as the apiculture industry in Hawai‘i.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Rusert, Lauren M. and Pettis, Jeffrey S. and Tarpy, David R.}, year={2021}, month={Jan} }
@article{mcafee_tarpy_foster_2021, title={Queen honey bees exhibit variable resilience to temperature stress}, volume={16}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0255381}, abstractNote={Extreme temperature exposure can reduce stored sperm viability within queen honey bees; however, little is known about how thermal stress may directly impact queen performance or other maternal quality metrics. Here, in a blind field trial, we recorded laying pattern, queen mass, and average callow worker mass before and after exposing queens to a cold temperature (4°C, 2 h), hot temperature (42°C, 2 h), and hive temperature (33°C, control). We measured sperm viability at experiment termination, and investigated potential vertical effects of maternal temperature stress on embryos using proteomics. We found that cold stress, but not heat stress, reduced stored sperm viability; however, we found no significant effect of temperature stress on any other recorded metrics (queen mass, average callow worker mass, laying patterns, the egg proteome, and queen spermathecal fluid proteome). Previously determined candidate heat and cold stress biomarkers were not differentially expressed in stressed queens, indicating that these markers only have short-term post-stress diagnostic utility. Combined with variable sperm viability responses to temperature stress reported in different studies, these data also suggest that there is substantial variation in temperature tolerance, with respect to impacts on fertility, amongst queens. Future research should aim to quantify the variation and heritability of temperature tolerance, particularly heat, in different populations of queens in an effort to promote queen resilience.}, number={8}, journal={PLOS ONE}, author={McAfee, Alison and Tarpy, David R. and Foster, Leonard J.}, year={2021} }
@article{metz_tarpy_2021, title={Reproductive and Morphological Quality of Commercial Honey Bee (Hymenoptera: Apidae) Drones in the United States}, volume={21}, ISSN={["1536-2442"]}, DOI={10.1093/jisesa/ieab048}, abstractNote={Abstract
Exploration into reproductive quality in honey bees (Apis mellifera Linneaus (Hymenoptera: Apidae) largely focuses on factors that affect queens, with drones primarily being considered insofar as they pass on effects of environmental stressors to the queen and subsequent offspring. In those studies that consider drone quality explicitly, a primary focus has been on the dimorphic nature of drones laid in worker cells (either through rare queen error or worker reproduction) as compared to drones laid by the queen in the slightly larger drone cells. The implication from these studies is that that there exists a bimodality of drone morphological quality that is related to reproductive quality and competitive ability during mating. Our study quantifies the presence of such small drones in commercial populations, finding that rates of ‘low-quality’ drones are far higher than theoretically predicted under optimum conditions. Observations from commercial colonies also show significant inter-colony variation among the size and fecundity of drones produced, prompting speculation as to the mechanisms inducing such variation and the potential use of drone-quality variation for the colony- or apiary-level exposure to nutrition, agrichemical, or parasitic stressors.}, number={6}, journal={JOURNAL OF INSECT SCIENCE}, author={Metz, Bradley N. and Tarpy, David R.}, year={2021}, month={Nov} }
@article{kulhanek_steinhauer_wilkes_wilson_spivak_sagili_tarpy_mcdermott_garavito_rennich_et al._2021, title={Survey-derived best management practices for backyard beekeepers improve colony health and reduce mortality}, volume={16}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0245490}, abstractNote={Honey bee colony losses in the US have exceeded acceptable levels for at least a decade, leaving beekeepers in need of management practices to improve colony health and survival. Here, an empirical Best Management Practice (BMP) regimen was tested, comprised of the top four management practices associated with reduced colony mortality in backyard beekeeping operations according to Bee Informed Partnership Loss and Management survey results. Seven study locations were established across the US, and each location consisted of ten colonies treated according to empirical BMPs and ten according to average beekeeping practice. After 3 years, colonies treated according to empirical BMPs experienced reduced Varroa infestation, viral infection, and mortality compared to colonies managed with Average practices. In addition, BMP colonies produced more new colonies via splits. The colonies under Average practices were given chemical Varroa treatments only once per year, and thus spent more months above economic threshold of 3.0 mites/100 bees. Increased time spent above the economic threshold was significantly correlated to both increased viral infection and colony mortality. This study demonstrates the cumulative effects of management and colony health stressors over months and years, especially the dire importance of regular Varroa monitoring and management.}, number={1}, journal={PLOS ONE}, author={Kulhanek, Kelly and Steinhauer, Nathalie and Wilkes, James and Wilson, Michaela and Spivak, Marla and Sagili, Ramesh R. and Tarpy, David R. and McDermott, Erin and Garavito, Andrew and Rennich, Karen and et al.}, year={2021}, month={Jan} }
@article{mcafee_chapman_pettis_foster_tarpy_2021, title={Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera)}, volume={4}, ISSN={["2399-3642"]}, DOI={10.1038/s42003-020-01586-w}, abstractNote={AbstractQueens of many social hymenoptera keep sperm alive within their specialized storage organ, the spermatheca, for years, defying the typical trade-off between lifespan and reproduction. However, whether honey bee (Apis mellifera) queens experience a trade-off between reproduction and immunity is unknown, and the biochemical processes underlying sperm viability are poorly understood. Here, we survey quality metrics and viral loads of honey bee queens from nine genetic sources. Queens rated as ‘failed’ by beekeepers had lower sperm viability, fewer sperm, and higher levels of sacbrood virus and black queen cell virus. Quantitative proteomics on N = 123 spermathecal fluid samples shows, after accounting for sperm count, health status, and apiary effects, five spermathecal fluid proteins significantly correlating with sperm viability: odorant binding protein (OBP)14, lysozyme, serpin 88Ea, artichoke, and heat-shock protein (HSP)10. The significant negative correlation of lysozyme—a conserved immune effector—with sperm viability is consistent with a reproduction vs. immunity trade-off in honey bee queens.}, number={1}, journal={COMMUNICATIONS BIOLOGY}, author={McAfee, Alison and Chapman, Abigail and Pettis, Jeffery S. and Foster, Leonard J. and Tarpy, David R.}, year={2021}, month={Jan} }
@article{mcafee_milone_chapman_foster_pettis_tarpy_2020, title={Candidate stress biomarkers for queen failure diagnostics}, volume={21}, ISSN={["1471-2164"]}, DOI={10.1186/s12864-020-06992-2}, abstractNote={Abstract
Background
Queen failure is a persistent problem in beekeeping operations, but in the absence of overt symptoms it is often difficult, if not impossible, to ascertain the root cause. Stressors like heat-shock, cold-shock, and sublethal pesticide exposure can reduce stored sperm viability and lead to cryptic queen failure. Previously, we suggested candidate protein markers indicating heat-shock in queens. Here, we further investigate these heat-shock markers and test new stressors to identify additional candidate protein markers.
Results
We found that heat-shocking queens for upwards of 1 h at 40 °C was necessary to induce significant changes in the two strongest candidate heat-shock markers, and that relative humidity significantly influenced the degree of activation. In blind heat-shock experiments, we tested the efficiency of these markers at assigning queens to their respective treatment groups and found that one marker was sufficient to correctly assign queens 75% of the time. Finally, we compared cold-shocked queens at 4 °C and pesticide-exposed queens to controls to identify candidate markers for these additional stressors, and compared relative abundances of all markers to queens designated as ‘healthy’ and ‘failing’ by beekeepers. Queens that failed in the field had higher expression of both heat-shock and pesticide protein markers, but not cold-shock markers.
Conclusions
This work offers some of the first steps towards developing molecular diagnostic tools to aid in determining cryptic causes of queen failure. Further work will be necessary to determine how long after the stress event a marker’s expression remains elevated, and how accurate these markers will be for field diagnoses.
}, number={1}, journal={BMC GENOMICS}, author={McAfee, Alison and Milone, Joseph and Chapman, Abigail and Foster, Leonard J. and Pettis, Jeffery S. and Tarpy, David R.}, year={2020}, month={Aug} }
@article{milone_chakrabarti_sagili_tarpy_2021, title={Colony-level pesticide exposure affects honey bee (Apis mellifera L.) royal jelly production and nutritional composition}, volume={263}, ISSN={["1879-1298"]}, DOI={10.1016/j.chemosphere.2020.128183}, abstractNote={Honey bees provision glandular secretions in the form of royal jelly as larval nourishment to developing queens. Exposure to chemicals and nutritional conditions can influence queen development and thus impact colony fitness. Previous research reports that royal jelly remains pesticide-free during colony-level exposure and that chemical residues are buffered by the nurse bees. However, the impacts of pesticides can also manifest in quality and quantity of royal jelly produced by nurse bees. Here, we tested how colony exposure to a multi-pesticide pollen treatment influences the amount of royal jelly provisioned per queen and the additional impacts on royal jelly nutritional quality. We observed differences in the metabolome, proteome, and phytosterol compositions of royal jelly synthesized by nurse bees from multi-pesticide exposed colonies, including significant reductions of key nutrients such as 24-methylenecholesterol, major royal jelly proteins, and 10-hydroxy-2-decenoic acid. Additionally, quantity of royal jelly provisioned per queen was lower in colonies exposed to pesticides, but this effect was colony-dependent. Pesticide treatment had a greater impact on royal jelly nutritional composition than the weight of royal jelly provisioned per queen cell. These novel findings highlight the indirect effects of pesticide exposure on queen developmental nutrition and allude to social consequences of nurse bee glandular degeneration.}, journal={CHEMOSPHERE}, author={Milone, Joseph P. and Chakrabarti, Priyadarshini and Sagili, Ramesh R. and Tarpy, David R.}, year={2021}, month={Jan} }
@article{milone_rinkevich_mcafee_foster_tarpy_2020, title={Differences in larval pesticide tolerance and esterase activity across honey bee (Apis mellifera) stocks}, volume={206}, ISSN={["1090-2414"]}, DOI={10.1016/j.ecoenv.2020.111213}, abstractNote={Honey bee populations in North America are an amalgamation of diverse progenitor ecotypes experiencing varying levels of artificial selection. Genetic differences between populations can result in variable susceptibility towards environmental stressors, and here we compared pesticide tolerances across breeding stocks using a mixture of seven pesticides frequently found in colonies providing pollination services. We administered the pesticide mixture chronically to in vitro reared larvae at four concentrations of increasing Hazard Quotient (HQ, or cumulative toxicity) and measured mortality during larval development. We found that different stocks had significantly different tolerances to our pesticide mixture as indicated by their median lethal toxicity (HQ50). The intensively selected Pol-Line stock exhibited the greatest pesticide sensitivity while Old World (progenitor) and putatively feral stocks were the most pesticide-tolerant. Furthermore, we found that activity of the detoxification enzyme esterase was positively correlated with pesticide tolerance when measured using two different substrate standards, and confirmed that larvae from the Pol-Line stock had generally lower esterase activity. Consistent with an increased pesticide tolerance, the Old World and putatively feral stocks had higher esterase activities. However, esterases and other detoxification enzymes (CYP450s and GSTs) were found in similar abundances across stocks, suggesting that the differences in enzyme activity we observed might arise from stock-specific single nucleotide polymorphisms or post-translational modifications causing qualitative variation in enzyme activity. These results suggest that selective breeding may inadvertently increase honey bees’ sensitivity to pesticides, whereas unselected, putatively feral and Old World stocks have larvae that are more tolerant.}, journal={ECOTOXICOLOGY AND ENVIRONMENTAL SAFETY}, author={Milone, Joseph P. and Rinkevich, Frank D. and McAfee, Alison and Foster, Leonard J. and Tarpy, David R.}, year={2020}, month={Dec} }
@article{amiri_herman_strand_tarpy_rueppell_2020, title={Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera}, volume={85}, ISSN={["1567-7257"]}, DOI={10.1016/j.meegid.2020.104558}, abstractNote={Trans-generational disease effects include vertical pathogen transmission but also immune priming to enhance offspring immunity. Accordingly, the survival consequences of maternal virus infection can vary and its molecular consequences during early development are poorly understood. The honey bee queen is long-lived and represents the central hub for vertical virus transmission as the sole reproductive individual in her colony. Even though virus symptoms in queens are mild, viral infection may have severe consequences for the offspring. Thus, transcriptome patterns during early developmental are predicted to respond to maternal virus infection. To test this hypothesis, gene expression patterns were compared among pooled honey bee eggs laid by queens that were either infected with Deformed wing virus (DWV1), Sacbrood virus (SBV2), both viruses (DWV and SBV), or no virus. Whole transcriptome analyses revealed significant expression differences of a few genes, some of which have hitherto no known function. Despite the paucity of single gene effects, functional enrichment analyses revealed numerous biological processes in the embryos to be affected by virus infection. Effects on several regulatory pathways were consistent with maternal responses to virus infection and correlated with responses to DWV and SBV in honey bee larvae and pupae. Overall, effects on egg transcriptome patterns were specific to each virus and the results of dual-infection samples suggested synergistic effects of DWV and SBV. We interpret our results as consequences of maternal infections. Thus, this first study to document and characterize virus-associated changes in the transcriptome of honey bee eggs represents an important contribution to understanding trans-generational virus effects, although more in-depth studies are needed to understand the detailed mechanisms of how viruses affect honey bee embryos.}, journal={INFECTION GENETICS AND EVOLUTION}, author={Amiri, Esmaeil and Herman, Jacob J. and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2020}, month={Nov} }
@article{amiri_le_melendez_strand_tarpy_rueppell_2020, title={Egg-size plasticity in Apis mellifera: Honey bee queens alter egg size in response to both genetic and environmental factors}, volume={33}, ISSN={["1420-9101"]}, DOI={10.1111/jeb.13589}, abstractNote={AbstractSocial evolution has led to distinct life‐history patterns in social insects, but many colony‐level and individual traits, such as egg size, are not sufficiently understood. Thus, a series of experiments was performed to study the effects of genotypes, colony size and colony nutrition on variation in egg size produced by honey bee (Apis mellifera) queens. Queens from different genetic stocks produced significantly different egg sizes under similar environmental conditions, indicating standing genetic variation for egg size that allows for adaptive evolutionary change. Further investigations revealed that eggs produced by queens in large colonies were consistently smaller than eggs produced in small colonies, and queens dynamically adjusted egg size in relation to colony size. Similarly, queens increased egg size in response to food deprivation. These results could not be solely explained by different numbers of eggs produced in the different circumstances but instead seem to reflect an active adjustment of resource allocation by the queen in response to colony conditions. As a result, larger eggs experienced higher subsequent survival than smaller eggs, suggesting that honey bee queens might increase egg size under unfavourable conditions to enhance brood survival and to minimize costly brood care of eggs that fail to successfully develop, and thus conserve energy at the colony level. The extensive plasticity and genetic variation of egg size in honey bees has important implications for understanding life‐history evolution in a social context and implies this neglected life‐history stage in honey bees may have trans‐generational effects.}, number={4}, journal={JOURNAL OF EVOLUTIONARY BIOLOGY}, author={Amiri, Esmaeil and Le, Kevin and Melendez, Carlos Vega and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2020}, month={Apr}, pages={534–543} }
@article{amiri_strand_tarpy_rueppell_2020, title={Honey Bee Queens and Virus Infections}, url={https://www.mdpi.com/1999-4915/12/3/322}, DOI={10.3390/v12030322}, abstractNote={The honey bee queen is the central hub of a colony to produce eggs and release pheromones to maintain social cohesion. Among many environmental stresses, viruses are a major concern to compromise the queen’s health and reproductive vigor. Viruses have evolved numerous strategies to infect queens either via vertical transmission from the queens’ parents or horizontally through the worker and drones with which she is in contact during development, while mating, and in the reproductive period in the colony. Over 30 viruses have been discovered from honey bees but only few studies exist on the pathogenicity and direct impact of viruses on the queen’s phenotype. An apparent lack of virus symptoms and practical problems are partly to blame for the lack of studies, and we hope to stimulate new research and methodological approaches. To illustrate the problems, we describe a study on sublethal effects of Israeli Acute Paralysis Virus (IAPV) that led to inconclusive results. We conclude by discussing the most crucial methodological considerations and novel approaches for studying the interactions between honey bee viruses and their interactions with queen health.}, journal={Viruses}, author={Amiri, Esmaeil and Strand, Micheline K. and Tarpy, David and Rueppell, Olav}, year={2020}, month={Mar} }
@article{kevill_lee_goblirsch_mcdermott_tarpy_spivak_schroeder_2020, title={The Pathogen Profile of a Honey Bee Queen Does Not Reflect That of Her Workers}, url={https://www.mdpi.com/2075-4450/11/6/382}, DOI={10.3390/insects11060382}, abstractNote={Throughout a honey bee queen’s lifetime, she is tended to by her worker daughters, who feed and groom her. Such interactions provide possible horizontal transmission routes for pathogens from the workers to the queen, and as such a queen’s pathogen profile may be representative of the workers within a colony. To explore this further, we investigated known honey bee pathogen co-occurrence, as well as pathogen transmission from workers to queens. Queens from 42 colonies were removed from their source hives and exchanged into a second, unrelated foster colony. Worker samples were taken from the source colony on the day of queen exchange and the queens were collected 24 days after introduction. All samples were screened for Nosema spp., Trypanosome spp., acute bee paralysis virus (ABPV), black queen cell virus (BQCV), chronic bee paralysis virus (CBPV), Israeli acute paralysis virus (IAPV), Lake Sinai virus (LSV), and deformed wing virus master variants (DWV-A, B, and C) using RT-qPCR. The data show that LSV, Nosema, and DWV-B were the most abundant pathogens in colonies. All workers (n = 42) were LSV-positive, 88% were Nosema-positive, whilst pathogen loads were low (<1 × 106 genome equivalents per pooled worker sample). All queens (n = 39) were negative for both LSV and Nosema. We found no evidence of DWV transmission occurring from worker to queen when comparing queens to foster colonies, despite DWV being present in both queens and workers. Honey bee pathogen presence and diversity in queens cannot be revealed from screening workers, nor were pathogens successfully transmitted to the queen.}, journal={Insects}, author={Kevill, Jessica and Lee, Katie and Goblirsch, Michael and McDermott, Erin and Tarpy, David and Spivak, Marla and Schroeder, Declan}, year={2020}, month={Jun} }
@article{li-byarlay_boncristiani_howell_herman_clark_strand_tarpy_rueppell_2020, title={Transcriptomic and Epigenomic Dynamics of Honey Bees in Response to Lethal Viral Infection}, volume={11}, ISSN={["1664-8021"]}, DOI={10.3389/fgene.2020.566320}, abstractNote={Honey bees (Apis mellifera L) suffer from many brood pathogens, including viruses. Despite considerable research, the molecular responses and dynamics of honey bee pupae to viral pathogens remain poorly understood. Israeli Acute Paralysis Virus (IAPV) is emerging as a model virus since its association with severe colony losses. Using worker pupae, we studied the transcriptomic and methylomic consequences of IAPV infection over three distinct time points after inoculation. Contrasts of gene expression and 5mC DNA methylation profiles between IAPV-infected and control individuals at these time points—corresponding to the pre-replicative (5 hr), replicative (20 hr), and terminal (48 hr) phase of infection—indicate that profound immune responses and distinct manipulation of host molecular processes accompany the lethal progression of this virus. We identify the temporal dynamics of the transcriptomic response to with more genes differentially expressed in the replicative and terminal phases than in the pre-replicative phase. However, the number of differentially methylated regions decreased dramatically from the pre-replicative to the replicative and terminal phase. Several cellular pathways experienced hyper- and hypo-methylation in the pre-replicative phase and later dramatically increased in gene expression at the terminal phase, including the MAPK, Jak-STAT, Hippo, mTOR, TGF-beta signaling pathways, ubiquitin mediated proteolysis, and spliceosome. These affected biological functions suggest that adaptive host responses to combat the virus are mixed with viral manipulations of the host to increase its own reproduction, all of which are involved in anti-viral immune response, cell growth, and proliferation. Comparative genomic analyses with other studies of viral infections of honey bees and fruit flies indicated that similar immune pathways are shared. Our results further suggest that dynamic DNA methylation responds to viral infections quickly, regulating subsequent gene activities. Our study provides new insights of molecular mechanisms involved in epigenetic that can serve as foundation for the long-term goal to develop anti-viral strategies for honey bees, the most important commercial pollinator. Author Summary Honey bees, the most important managed pollinators, are experiencing unsustainable mortality. Israeli Acute Paralysis Virus (IAPV) causes economically important disease in honey bees, and it is emerging as a model system to study viral pathogen-host interactions in pollinators. The pupation stage is important for bee development but individuals are particularly vulnerable for parasitic mite infestations and viral infections. Currently, it is unclear how honey bee pupae respond to this virus. However, these responses, including gene expression and DNA methylomic changes, are critical to understand so that anti-viral genes can be identified and new anti-viral strategies be developed. Here, we use next-generation sequencing tools to reveal the dynamic changes of gene expression and DNA methylation as pupae succumb to IAPV infections after 5, 20, and 48 hours. We found that IAPV causes changes in regions of DNA methylation more at the beginning of infection than later. The activity of several common insect immune pathways are affected by the IAPV infections, as are some other fundamental biological processes. Expression of critical enzymes in DNA methylation are also induced by IAPV in a temporal manner. By comparing our results to other virus studies of honey bees and fruit flies, we identified common anti-viral immune responses. Thus, our study provides new insight on the genome responses of honey bees over the course of a fatal virus infection with theoretical and practical implications.}, journal={FRONTIERS IN GENETICS}, author={Li-Byarlay, Hongmei and Boncristiani, Humberto and Howell, Gary and Herman, Jake and Clark, Lindsay and Strand, Micheline K. and Tarpy, David and Rueppell, Olav}, year={2020}, month={Sep} }
@article{mcafee_chapman_higo_underwood_milone_foster_guarna_tarpy_pettis_2020, title={Vulnerability of honey bee queens to heat-induced loss of fertility}, volume={3}, ISSN={["2398-9629"]}, DOI={10.1038/s41893-020-0493-x}, abstractNote={All species need to reproduce to maintain viable populations, but heat stress kills sperm cells across the animal kingdom and rising frequencies of heat waves are a threat to biodiversity. Honey bees (Apis mellifera) are globally distributed microlivestock; therefore, they could serve as environmental biomonitors for fertility losses. Here, we found that queens have two potential routes of temperature-stress exposure: within colonies and during routine shipping. Our data suggest that temperatures of 15–38 °C are safe for queens at a tolerance threshold of 11.5% loss of sperm viability, which is the viability difference associated with queen failure in the field. Heat shock activates expression of specific stress-response proteins in the spermatheca, which could serve as molecular biomarkers (indicators) for heat stress. This protein fingerprint may eventually enable surveys for the prevalence of heat-induced loss of sperm viability in diverse landscapes as part of a biomonitoring programme. Heat waves can pose a threat to biodiversity as heat stress kills sperm cells across the animal kingdom. Here, honey bee queens are found to be vulnerable to temperature changes and the specific stress-response proteins activated in the spermatheca are discussed as potential indicators of heat stress.}, number={5}, journal={NATURE SUSTAINABILITY}, author={McAfee, Alison and Chapman, Abigail and Higo, Heather and Underwood, Robyn and Milone, Joseph and Foster, Leonard J. and Guarna, M. Marta and Tarpy, David R. and Pettis, Jeffery S.}, year={2020}, month={May}, pages={367–376} }
@article{giuffre_lubkin_tarpy_2019, title={Does viral load alter behavior of the bee parasite Varroa destructor?}, volume={14}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0217975}, abstractNote={The invasive mite Varroa destructor has negatively impacted global apiculture, by being a vector for many viruses of the honey bee (Apis mellifera). Until now, most studies have been limited to varroa-honey bee or virus-honey bee interactions. The aim of this study is to bridge the important research gap of varroa-virus interactions by correlating varroa behavior with viral load. Ten-minute video recordings of 200 varroa mites were analyzed, and average speeds of the mites were compared to individual qPCR viral loads for deformed wing virus (DWV) and sacbrood virus (SBV). Statistically significant models reveal that colony, DWV, and SBV all might play a role in mite behavior, suggesting that the varroa-virus interaction needs to be an integral part of future studies on honey bee pathogens.}, number={6}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Giuffre, Carl and Lubkin, Sharon R. and Tarpy, David R.}, editor={Rueppell, OlavEditor}, year={2019}, month={Jun} }
@article{withrow_pettis_tarpy_2019, title={Effects of Temperature During Package Transportation on Queen Establishment and Survival in Honey Bees (Hymenoptera: Apidae)}, volume={112}, ISSN={["1938-291X"]}, DOI={10.1093/jee/toz003}, abstractNote={Honey bee (Apis mellifera) (Linnaeus) (Hymenoptera: Apidae) queens, the reproductive female caste, are crucial for colony success, and many management problems that beekeepers face are related to their diminished reproductive quality and premature failure. Previous research has suggested that temperature extremes may affect the viability of stored sperm in queens' spermathecae, thus the abiotic conditions of queens during transport may be germane to these problems. We recorded the temperatures experienced by queens during 2 yr of package transportation and tracked the newly installed colonies through establishment and buildup. During this critical 6-8 wk period, we observed typically high rates of queen failure (~25%) but found no indication that these postinstallation queen events were driven by temperature-related damage to stored sperm (an essential component of queen quality) incurred during transportation. We also found no indication of significant hot or cold zones across the truckloads of packages that would suggest a problem in how packages are insulated during transportation. However, we did observe significantly higher temperatures (31.2 vs. 29.9°C) and lower temperature variance (8.8 vs. 12.2) in queens that ultimately failed during the observation period, indicating that workers may respond differently to these queens in a way that manifests as more insulating clusters around queen cages. If so, then the collective process by which workers accept or reject a foreign queen may already be detectable even if it does not ultimately conclude until some weeks later. Nevertheless, it remains unclear why large numbers of otherwise high-quality queens are failing in newly installed packages.}, number={3}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Withrow, James M. and Pettis, Jeffery S. and Tarpy, David R.}, year={2019}, month={Jun}, pages={1043–1049} }
@article{de souza_hartfelder_tarpy_2019, title={Effects of larval Age at Grafting and Juvenile Hormone on Morphometry and Reproductive Quality Parameters of in Vitro Reared Honey Bees (Hymenoptera: Apidae)}, volume={112}, ISSN={["1938-291X"]}, DOI={10.1093/jee/toz148}, abstractNote={AbstractThe honey bee queen plays a central role in the Apis mellifera L. (Hymenoptera: Apidae) colony, and her high reproductive capacity is fundamental for building up the workforce of a colony. Caste development in honey bee females involves elaborate physiological pathways unleashed at the beginning of the first larval instars, with juvenile hormone (JH) playing a crucial role. Here we took advantage of established in vitro rearing techniques to conduct a 2 × 2 experimental design and test initial rearing age (young vs old) and JH treatment (JH III vs solvent control) to enlighten the role of nutrient quality and JH in shaping honey bee female fertility, morphological features related to queenliness, and key physiological parameters (hemolymph vitellogenin/Vg, sugar levels, and Vg transcript levels). Our results show that while the age at initial larval rearing had major impacts on external morphology development, where younger larvae exhibited a higher probability to develop into queen-like adults morphotypes, the JH application during the larval stage improved physiological pathways related to ovary development and metabolism during the ontogenic development. We detected that the supplementation of queen larvae with JH promoted important benefits regarding queen fertility as the increase of ovariole number and vg levels at hemolymph, both crucial factors at eggs production. The data presented here provide guidance in efforts to improve honey bee queen quality, especially in light of frequent episodes of queen failures in the beekeeping industry.}, number={5}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={De Souza, Daiana A. and Hartfelder, Klaus H. and Tarpy, David R.}, year={2019}, month={Oct}, pages={2030–2039} }
@article{mcafee_pettis_tarpy_foster_2019, title={Feminizer and doublesex knock-outs cause honey bees to switch sexes}, volume={17}, ISSN={["1545-7885"]}, DOI={10.1371/journal.pbio.3000256}, abstractNote={Honey bees are experts at refuting societal norms. Their matriarchal hives are headed by queens, backed by an all-female workforce, and males die soon after copulation. But the biochemical basis of how these distinct castes and sexes (queens, workers, and drones) arise is poorly understood, partly due to a lack of efficient tools for genetic manipulation. Now, Roth and colleagues have used clustered regularly interspaced short palindromic repeats (CRISPR) to knock out two key genes (feminizer and doublesex) that guide sexual development. Their technique yielded remarkably low rates of genetic mosaicism and offers a promising tool for engineering and phenotyping bees for diverse applications.}, number={5}, journal={PLOS BIOLOGY}, author={McAfee, Alison and Pettis, Jeffery S. and Tarpy, David R. and Foster, Leonard J.}, year={2019}, month={May} }
@article{lee_goblirsch_mcdermott_tarpy_spivak_2019, title={Is the Brood Pattern within a Honey Bee Colony a Reliable Indicator of Queen Quality?}, volume={10}, ISSN={["2075-4450"]}, url={http://www.mdpi.com/2075-4450/10/1/12}, DOI={10.3390/insects10010012}, abstractNote={Failure of the queen is often identified as a leading cause of honey bee colony mortality. However, the factors that can contribute to “queen failure” are poorly defined and often misunderstood. We studied one specific sign attributed to queen failure: poor brood pattern. In 2016 and 2017, we identified pairs of colonies with “good” and “poor” brood patterns in commercial beekeeping operations and used standard metrics to assess queen and colony health. We found no queen quality measures reliably associated with poor-brood colonies. In the second year (2017), we exchanged queens between colony pairs (n = 21): a queen from a poor-brood colony was introduced into a good-brood colony and vice versa. We observed that brood patterns of queens originally from poor-brood colonies significantly improved after placement into a good-brood colony after 21 days, suggesting factors other than the queen contributed to brood pattern. Our study challenges the notion that brood pattern alone is sufficient to judge queen quality. Our results emphasize the challenges in determining the root source for problems related to the queen when assessing honey bee colony health.}, number={1}, journal={INSECTS}, author={Lee, Kathleen V. and Goblirsch, Michael and McDermott, Erin and Tarpy, David R. and Spivak, Marla}, year={2019}, month={Jan} }
@article{amiri_seddon_smith_strand_tarpy_rueppell_2019, title={Israeli Acute Paralysis Virus: Honey Bee Queen-Worker Interaction and Potential Virus Transmission Pathways}, volume={10}, ISSN={["2075-4450"]}, DOI={10.3390/insects10010009}, abstractNote={Queen loss or failure is an important cause of honey bee colony loss. A functional queen is essential to a colony, and the queen is predicted to be well protected by worker bees and other mechanisms of social immunity. Nevertheless, several honey bee pathogens (including viruses) can infect queens. Here, we report a series of experiments to test how virus infection influences queen–worker interactions and the consequences for virus transmission. We used Israeli acute paralysis virus (IAPV) as an experimental pathogen because it is relevant to bee health but is not omnipresent. Queens were observed spending 50% of their time with healthy workers, 32% with infected workers, and 18% without interaction. However, the overall bias toward healthy workers was not statistically significant, and there was considerable individual to individual variability. We found that physical contact between infected workers and queens leads to high queen infection in some cases, suggesting that IAPV infections also spread through close bodily contact. Across experiments, queens exhibited lower IAPV titers than surrounding workers. Thus, our results indicate that honey bee queens are better protected by individual and social immunity, but this protection is insufficient to prevent IAPV infections completely.}, number={1}, journal={INSECTS}, author={Amiri, Esmaeil and Seddon, Gregory and Smith, Wendy Zuluaga and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2019}, month={Jan} }
@article{amiri_seddon_smith_strand_tarpy_rueppell_2019, title={Israeli Acute Paralysis Virus: Honey Bee Queen-Worker Interaction and Potential Virus Transmission Pathways (vol 10, 9, 2019)}, volume={10}, ISSN={["2075-4450"]}, DOI={10.3390/insects10050123}, abstractNote={It has been brought to our attention that one note was missing in the Funding section of our published paper [...]}, number={5}, journal={INSECTS}, author={Amiri, Esmaeil and Seddon, Gregory and Smith, Wendy Zuluaga and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2019}, month={May} }
@article{metz_tarpy_2019, title={Reproductive Senescence in Drones of the Honey Bee (Apis mellifera)}, volume={10}, ISSN={["2075-4450"]}, DOI={10.3390/insects10010011}, abstractNote={In the face of high proportions of yearly colony losses, queen health and fecundity has been a major focus of industry and research. Much of the reproductive quality of the queen, though, is a function of the mating success and quality of the drones (males). Many environmental factors can negatively impact drone semen quality, but little is known about factors that impact the drones’ ability to successfully mate and deliver that semen, or how widely drones vary. In our study, we observed the daily variation in honey bee drone reproductive quality over time, along with a number of morphological traits. Drones were reared in cages in bank colonies, and 20 individuals were dissected and measured daily. The number of viable spermatozoa in the seminal vesicles was zero at emergence and reached an average maximum of 7.39 ± 0.19 million around 20 days of life. Decline in spermatozoa count occurred after day 30, though viability was constant throughout life, when controlling for count. Older drones had smaller wet weights, head widths, and wing lengths. We predict that this is likely due to sampling bias due to a differential lifespan among larger, more reproductively developed drones. Our study shows that drones are more highly variable than previously suggested and that they have a significant variation in reproductive physiology as a function of age.}, number={1}, journal={INSECTS}, author={Metz, Bradley N. and Tarpy, David R.}, year={2019}, month={Jan} }
@article{withrow_tarpy_2018, title={Cryptic "royal" subfamilies in honey bee (Apis mellifera) colonies}, volume={13}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0199124}, abstractNote={During emergency queen rearing, worker honey bees (Apis mellifera) select several otherwise worker-destined larvae to instead rear as candidates to replace their dead or failing queen. This choice is crucial as the queen is the sole reproductive in the colony and her quality is essential to its success. Because honey bee queens mate with and store sperm from multiple drones, emergency queen selection presents workers with an opportunity to increase fitness by selecting full- (0.75 relatedness), rather than half- (0.25 relatedness), sisters as new queen candidates. Through patriline analysis of colonies along with large numbers of emergency queens reared by each we affirm the purported “royal” patriline theory that, instead of competing nepotistically, workers exhibit bias towards selecting individuals from particular “royal” subfamilies during emergency queen rearing events, Further, we show that these “royal” patrilines are cryptic in honey bee colonies; occurring in such low frequency in the overall colony population that they are frequently undetected in traditional tests of queen mating number and colony composition. The identification of these cryptic “royal” subfamilies reveals that honey bee queens, already considered “hyperpolyandrous,” are mating with even more males than has been previously recognized. These results alter our understanding of reproductive behavior in honey bees, raising questions about the evolutionary implications of this phenomenon.}, number={7}, journal={PLOS ONE}, author={Withrow, James M. and Tarpy, David R.}, year={2018}, month={Jul} }
@article{de souza_huang_tarpy_2019, title={Experimental improvement of honey bee (Apis mellifera) queen quality through nutritional and hormonal supplementation}, volume={50}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-018-0614-y}, abstractNote={Queen reproductive potential (=quality) impacts the health and productivity of honey bee colonies. To determine the factors that affect reproductive quality during development, we tested queens produced under larval treatments by supplementing the diet with juvenile hormone (JH), additional sugars, or both, compared to untreated control. Furthermore, we varied the age of the larvae that were grafted (1 and 3 days old). We analyzed newly emerged virgin queens for their morphological characters as proxies for their reproductive potential. We found that the application of a sugar-enriched diet in combination with JH application onto 1st instar queen larvae produced higher-quality queens, while for 3rd instar larvae only the JH treatment resulted in increasing queen quality. For mated queens, those treated with JH plus supplemented sugars showed a significantly higher sperm count and sperm viability. Our findings demonstrate that honey bee queen reproductive potential can be increased through diet supplementation.}, number={1}, journal={APIDOLOGIE}, author={De Souza, Daiana A. and Huang, Ming Hua and Tarpy, David R.}, year={2019}, month={Feb}, pages={14–27} }
@article{simone-finstrom_tarpy_2018, title={Honey Bee Queens Do Not Count Mates to Assess their Mating Success}, volume={31}, ISSN={["1572-8889"]}, DOI={10.1007/s10905-018-9671-3}, number={2}, journal={JOURNAL OF INSECT BEHAVIOR}, author={Simone-Finstrom, Michael and Tarpy, David R.}, year={2018}, month={Mar}, pages={200–209} }
@article{alburaki_chen_skinner_meikle_tarpy_adamczyk_stewart_2018, title={Honey Bee Survival and Pathogen Prevalence: From the Perspective of Landscape and Exposure to Pesticides}, volume={9}, ISSN={["2075-4450"]}, DOI={10.3390/insects9020065}, abstractNote={In order to study the in situ effects of the agricultural landscape and exposure to pesticides on honey bee health, sixteen honey bee colonies were placed in four different agricultural landscapes. Those landscapes were three agricultural areas with varying levels of agricultural intensity (AG areas) and one non-agricultural area (NAG area). Colonies were monitored for different pathogen prevalence and pesticide residues over a period of one year. RT-qPCR was used to study the prevalence of seven different honey bee viruses as well as Nosema sp. in colonies located in different agricultural systems with various intensities of soybean, corn, sorghum, and cotton production. Populations of the parasitic mite Varroa destructor were also extensively monitored. Comprehensive MS-LC pesticide residue analyses were performed on samples of wax, honey, foragers, winter bees, dead bees, and crop flowers for each apiary and location. A significantly higher level of varroa loads were recorded in colonies of the AG areas, but this at least partly correlated with increased colony size and did not necessarily result from exposure to pesticides. Infections of two viruses (deformed wing virus genotype a (DWVa) and acute bee paralysis virus (ABPV)) and Nosema sp. varied among the four studied locations. The urban location significantly elevated colony pathogen loads, while AG locations significantly benefited and increased the colony weight gain. Cotton and sorghum flowers contained high concentrations of insecticide including neonicotinoids, while soybean and corn had less pesticide residues. Several events of pesticide toxicity were recorded in the AG areas, and high concentrations of neonicotinoid insecticides were detected in dead bees.}, number={2}, journal={INSECTS}, author={Alburaki, Mohamed and Chen, Deniz and Skinner, John A. and Meikle, William G. and Tarpy, David R. and Adamczyk, John and Stewart, Scott D.}, year={2018}, month={Jun} }
@article{giacomini_leslie_tarpy_palmer-young_irwin_adler_2018, title={Medicinal value of sunflower pollen against bee pathogens}, volume={8}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/s41598-018-32681-y}, DOI={10.1038/s41598-018-32681-y}, abstractNote={AbstractGlobal declines in pollinators, including bees, can have major consequences for ecosystem services. Bees are dominant pollinators, making it imperative to mitigate declines. Pathogens are strongly implicated in the decline of native and honey bees. Diet affects bee immune responses, suggesting the potential for floral resources to provide natural resistance to pathogens. We discovered that sunflower (Helianthus annuus) pollen dramatically and consistently reduced a protozoan pathogen (Crithidia bombi) infection in bumble bees (Bombus impatiens) and also reduced a microsporidian pathogen (Nosema ceranae) of the European honey bee (Apis mellifera), indicating the potential for broad anti-parasitic effects. In a field survey, bumble bees from farms with more sunflower area had lower Crithidia infection rates. Given consistent effects of sunflower in reducing pathogens, planting sunflower in agroecosystems and native habitat may provide a simple solution to reduce disease and improve the health of economically and ecologically important pollinators.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Giacomini, Jonathan J. and Leslie, Jessica and Tarpy, David R. and Palmer-Young, Evan C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2018}, month={Sep} }
@article{amiri_kryger_meixner_strand_tarpy_rueppell_2018, title={Quantitative patterns of vertical transmission of deformed wing virus in honey bees}, volume={13}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0195283}, abstractNote={Deformed wing virus (DWV) is an important pathogen in a broad range of insects, including honey bees. Concordant with the spread of Varroa, DWV is present in the majority of honey bee colonies and can result in either low-level infections with asymptomatic bees that nonetheless exhibit increased colony loss under stress, or high-level infections with acute effects on bee health and viability. DWV can be transmitted vertically or horizontally and evidence suggests that horizontal transmission via Varroa is associated with acute symptomatic infections. Vertical transmission also occurs and is presumably important for the maintenance of DWV in honey bee populations. To further our understanding the vertical transmission of DWV through queens, we performed three experiments: we studied the quantitative effectiveness of vertical transmission, surveyed the prevalence of successful egg infection under commercial conditions, and distinguished among three possible mechanisms of transmission. We find that queen-infection level predicts the DWV titers in their eggs, although the transmission is not very efficient. Our quantitative assessment of DWV demonstrates that eggs in 1/3 of the colonies are infected with DWV and highly infected eggs are rare in newly-installed spring colonies. Additionally, our results indicate that DWV transmission occurs predominantly by virus adhering to the surface of eggs (transovum) rather than intracellularly. Our combined results suggest that the queens’ DWV vectoring capacity in practice is not as high as its theoretical potential. Thus, DWV transmission by honey bee queens is part of the DWV epidemic with relevant practical implications, which should be further studied.}, number={3}, journal={PLOS ONE}, author={Amiri, Esmaeil and Kryger, Per and Meixner, Marina D. and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2018}, month={Mar} }
@article{kulhanek_steinhauer_rennich_caron_sagili_pettis_ellis_wilson_wilkes_tarpy_et al._2017, title={A national survey of managed honey bee 2015-2016 annual colony losses in the USA}, volume={56}, ISSN={["2078-6913"]}, DOI={10.1080/00218839.2017.1344496}, abstractNote={Managed honey bee colony losses are of concern in the USA and globally. This survey, which documents the rate of colony loss in the USA during the 2015–2016 season, is the tenth report of winter losses, and the fifth of summer and annual losses. Our results summarize the responses of 5725 valid survey respondents, who collectively managed 427,652 colonies on 1 October 2015, an estimated 16.1% of all managed colonies in the USA. Responding beekeepers reported a total annual colony loss of 40.5% [95% CI 39.8–41.1%] between 1 April 2015 and 1 April 2016. Total winter colony loss was 26.9% [95% CI 26.4–27.4%] while total summer colony loss was 23.6% [95% CI 23.0–24.1%], making this the third consecutive year when summer losses have approximated to winter losses. Across all operation types, 32.3% of responding beekeepers reported no winter losses. Whilst the loss rate in the winter of 2015–2016 was amongst the lowest winter losses recorded over the ten years this survey has been conducted, 59.0% (n = 3378) of responding beekeepers had higher losses than they deemed acceptable.}, number={4}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Kulhanek, Kelly and Steinhauer, Nathalie and Rennich, Karen and Caron, Dewey M. and Sagili, Ramesh R. and Pettis, Jeff S. and Ellis, James D. and Wilson, Michael E. and Wilkes, James T. and Tarpy, David R. and et al.}, year={2017}, pages={328–340} }
@article{alburaki_steckel_williams_skinner_tarpy_meikle_adamczyk_stewart_2017, title={Agricultural Landscape and Pesticide Effects on Honey Bee (Hymenoptera: Apidae) Biological Traits}, volume={110}, ISSN={["1938-291X"]}, DOI={10.1093/jee/tox111}, abstractNote={Abstract
Sixteen honey bee (Apis mellifera L.) colonies were placed in four different agricultural landscapes to study the effects of agricultural landscape and exposure to pesticides on honey bee health. Colonies were located in three different agricultural areas with varying levels of agricultural intensity (AG areas) and one nonagricultural area (NAG area). Colonies were monitored for their performance and productivity for one year by measuring colony weight changes, brood production, and colony thermoregulation. Palynological and chemical analyses were conducted on the trapped pollen collected from each colony and location. Our results indicate that the landscape’s composition significantly affected honey bee colony performance and development. Colony weight and brood production were significantly greater in AG areas compared to the NAG area. Better colony thermoregulation in AG areas’ colonies was also observed. The quantities of pesticides measured in the trapped pollen were relatively low compared to their acute toxicity. Unexplained queen and colony losses were recorded in the AG areas, while colony losses because of starvation were observed in the NAG area. Our results indicate that landscape with high urban activity enhances honey bee brood production, with no significant effects on colony weight gain. Our study indicates that agricultural crops provide a valuable resource for honey bee colonies, but there is a trade-off with an increased risk of exposure to pesticides.}, number={3}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Alburaki, Mohamed and Steckel, Sandra J. and Williams, Matthew T. and Skinner, John A. and Tarpy, David R. and Meikle, William G. and Adamczyk, John and Stewart, Scott D.}, year={2017}, month={Jun}, pages={835–847} }
@article{giuffre_lubkin_tarpy_2017, title={Automated assay and differential model of western honey bee (Apis mellifera) autogrooming using digital image processing}, volume={135}, ISSN={["1872-7107"]}, DOI={10.1016/j.compag.2017.02.003}, abstractNote={In animals, self-grooming is an important component of their overall hygiene because it reduces the risk of disease and parasites. The European honey bee (Apis mellifera) exhibits hygienic behavior, which refers to the ability of the members of a colony to remove diseased or dead brood from the hive. Individual grooming behavior, however, is when a bee grooms itself to remove parasites. While both behaviors are critical for the mitigation of disease, hygienic behavior is overwhelmingly more studied because, unlike grooming behavior, it has a simple bioassay to measure its phenotype. Here, we develop a novel bioassay to expedite data collection of grooming behavior by testing different honey bee genotypes (stocks). Individual worker bees from different commercial stocks were coated in baking flour, placed in an observation arena, and digitally recorded to automatically measure grooming rates. The videos were analyzed in MATLAB, and an exponential function was fit to the pixel data to calculate individual grooming rates. While bees from the different commercial stocks were not significantly different in their grooming rates, the automation of grooming measurements may facilitate future research and stock selection for this important mechanism of social immunity.}, journal={COMPUTERS AND ELECTRONICS IN AGRICULTURE}, publisher={Elsevier BV}, author={Giuffre, Carl and Lubkin, Sharon R. and Tarpy, David R.}, year={2017}, month={Apr}, pages={338–344} }
@article{mattos_soares_tarpy_2017, title={Effects of synthetic acaricides on honey bee grooming behavior against the parasitic Varroa destructor mite}, volume={48}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-017-0491-9}, abstractNote={Varroa destructor is currently one of the main threats for western apiculture. Today, synthetic acaricides (specifically coumaphos, amitraz, and tau-fluvalinate) are the most common methods to control Varroa infestations. These compounds, however, are frequently related to a wide range of side effects in the host, as well as a long half-life inside the hive matrices (wax and honey). The western honey bee, Apis mellifera, exhibits natural defense mechanisms against the mite such as grooming behavior, which is a sequence of bodily movements where the host scrapes its legs across its body surface to remove the mite. We tested the effects of synthetic acaricides on the performance of grooming behavior by adult honey bee workers. We found that acaricide exposure prior to grooming delayed grooming and reduced the overall duration of grooming behavior. Our data add to a list of other sublethal behavioral consequences of acaricides that may subvert a comprehensive approach to Varroa control in managed colonies.}, number={4}, journal={APIDOLOGIE}, author={Mattos, Igor Medici and Soares, Ademilson E. E. and Tarpy, David R.}, year={2017}, month={Jul}, pages={483–494} }
@article{lopez-uribe_appler_youngsteadt_dunn_frank_tarpy_2017, title={Higher immunocompetence is associated with higher genetic diversity in feral honey bee colonies (Apis mellifera)}, volume={18}, ISSN={["1572-9737"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85013371895&partnerID=MN8TOARS}, DOI={10.1007/s10592-017-0942-x}, number={3}, journal={CONSERVATION GENETICS}, author={Lopez-Uribe, Margarita M. and Appler, R. Holden and Youngsteadt, Elsa and Dunn, Robert R. and Frank, Steven D. and Tarpy, David R.}, year={2017}, month={Jun}, pages={659–666} }
@article{alburaki_steckel_chen_mcdermott_weiss_skinner_kelly_lorenz_tarpy_meikle_et al._2017, title={Landscape and pesticide effects on honey bees: forager survival and expression of acetylcholinesterase and brain oxidative genes}, volume={48}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-017-0497-3}, abstractNote={The aim of the present work was to assess the effects of landscape and pesticides on honey bee survival and physiological stress. Integrated use of acetylcholinesterase and detoxification enzymes was tested on honey bee brains for detecting possible exposure to pesticides. Foragers were tracked in agricultural and non-agricultural landscapes in West Tennessee (USA) and then recovered for molecular and chemical analyses. In addition, four honey bee cohorts were fed imidacloprid in the laboratory ad libitum for several weeks and were analyzed by RT-qPCR for gene expression. Pesticides were identified at different concentrations in both crop flowers and recovered foragers. No significant differences in foragers' mortality were found among locations. Acetylcholinesterase and detoxification genes showed no response to exposure to pesticides except for GstS3 and GstS4. Our results suggest that none of the studied genes make suitable biomarkers for honey bee exposed to pesticides.}, number={4}, journal={APIDOLOGIE}, author={Alburaki, Mohamed and Steckel, Sandra J. and Chen, Deniz and McDermott, Erin and Weiss, Milagra and Skinner, John A. and Kelly, Heather and Lorenz, Gus and Tarpy, David R. and Meikle, William G. and et al.}, year={2017}, month={Jul}, pages={556–571} }
@article{long_cao_keller_tarpy_shin_schneider_2017, title={Levels of selection shaping caste interactions during queen replacement in the honey bee, Apis mellifera}, volume={64}, ISSN={["1420-9098"]}, DOI={10.1007/s00040-016-0537-4}, number={2}, journal={INSECTES SOCIAUX}, author={Long, K. and Cao, T. T. and Keller, J. J. and Tarpy, D. R. and Shin, M. and Schneider, S. S.}, year={2017}, month={May}, pages={227–240} }
@article{mattos_soares_tarpy_2018, title={Mitigating effects of pollen during paraquat exposure on gene expression and pathogen prevalence in Apis mellifera L}, volume={27}, ISSN={["1573-3017"]}, DOI={10.1007/s10646-017-1868-2}, abstractNote={Honey bee (Apis mellifera L.) populations have been experiencing notable mortality in Europe and North America. No single cause has been identified for these dramatic losses, but rather multiple interacting factors are likely responsible (such as pesticides, malnutrition, habitat loss, and pathogens). Paraquat is one of the most widely used non-selective herbicides, especially in developing countries. This herbicide is considered slightly toxic to honey bees, despite being reported as a highly effective inducer of oxidative stress in a wide range of living systems. Here, we test the effects of paraquat on the expression of detoxification and antioxidant-related genes, as well as on the dynamics of pathogen titers. Moreover, we tested the effects of pollen as mitigating factor to paraquat exposure. Our results show significant changes in the expression of several antioxidant-related and detoxification-related genes in the presence of paraquat, as well as an increase of pathogens titers. Finally, we demonstrate a mitigating effect of pollen through the up-regulation of specific genes and improvement of survival of bees exposed to paraquat. The presence of pollen in the diet was also correlated with a reduced prevalence of Nosema and viral pathogens. We discuss the importance of honey bees' nutrition, especially the availability of pollen, on colony losses chronically reported in the USA and Europe.}, number={1}, journal={ECOTOXICOLOGY}, author={Mattos, Igor Medici and Soares, Ademilson E. E. and Tarpy, David R.}, year={2018}, month={Jan}, pages={32–44} }
@article{strange_delaney_tarpy_james_2017, title={Novel microsatellite loci reveal high genetic diversity yet low population structure for alfalfa leafcutting bees in North America}, volume={18}, ISSN={["1572-9737"]}, DOI={10.1007/s10592-017-0943-9}, number={3}, journal={CONSERVATION GENETICS}, author={Strange, James P. and Delaney, Deborah A. and Tarpy, David R. and James, Rosalind R.}, year={2017}, month={Jun}, pages={679–687} }
@misc{amiri_strand_rueppell_tarpy_2017, title={Queen Quality and the Impact of Honey Bee Diseases on Queen Health: Potential for Interactions between Two Major Threats to Colony Health}, volume={8}, ISSN={["2075-4450"]}, DOI={10.3390/insects8020048}, abstractNote={Western honey bees, Apis mellifera, live in highly eusocial colonies that are each typically headed by a single queen. The queen is the sole reproductive female in a healthy colony, and because long-term colony survival depends on her ability to produce a large number of offspring, queen health is essential for colony success. Honey bees have recently been experiencing considerable declines in colony health. Among a number of biotic and abiotic factors known to impact colony health, disease and queen failure are repeatedly reported as important factors underlying colony losses. Surprisingly, there are relatively few studies on the relationship and interaction between honey bee diseases and queen quality. It is critical to understand the negative impacts of pests and pathogens on queen health, how queen problems might enable disease, and how both factors influence colony health. Here, we review the current literature on queen reproductive potential and the impacts of honey bee parasites and pathogens on queens. We conclude by highlighting gaps in our knowledge on the combination of disease and queen failure to provide a perspective and prioritize further research to mitigate disease, improve queen quality, and ensure colony health.}, number={2}, journal={INSECTS}, author={Amiri, Esmaeil and Strand, Micheline K. and Rueppell, Olav and Tarpy, David R.}, year={2017}, month={Jun} }
@article{simone-finstrom_walz_tarpy_2016, title={Genetic diversity confers colony-level benefits due to individual immunity}, volume={12}, ISSN={["1744-957X"]}, DOI={10.1098/rsbl.2015.1007}, abstractNote={
Several costs and benefits arise as a consequence of eusociality and group-living. With increasing group size, spread of disease among nest-mates poses selective pressure on both individual immunity and group-level mechanisms of disease resistance (social immunity). Another factor known to influence colony-level expression of disease is intracolony genetic diversity, which in honeybees (
Apis mellifera
) is a direct function of the number of mates of the queen. Colonies headed by queens with higher mating numbers have less variable infections of decreased intensity, though the underlying mechanisms remain unclear. By pathogen-challenging larvae
in vitro
, we decoupled larval immune response from mechanisms of social immunity. Our results show that baseline immunity and degree of immune response do not vary with genetic diversity. However, intracolony variance in antimicrobial peptide production after pathogen challenge decreases with increasing genetic diversity. This reduction in variability of the larval immune response could drive the mitigation of disease observed in genetically diverse colonies.
}, number={3}, journal={BIOLOGY LETTERS}, author={Simone-Finstrom, Michael and Walz, Megan and Tarpy, David R.}, year={2016}, month={Mar} }
@article{rangel_böröczky_schal_tarpy_2016, title={Honey Bee (Apis mellifera) Queen Reproductive Potential Affects Queen Mandibular Gland Pheromone Composition and Worker Retinue Response}, volume={11}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0156027}, DOI={10.1371/journal.pone.0156027}, abstractNote={Reproductive division of labor is one of the defining traits of honey bees (Apis mellifera), with non-reproductive tasks being performed by workers while a single queen normally monopolizes reproduction. The decentralized organization of a honey bee colony is maintained in large part by a bouquet of queen-produced pheromones, the distribution of which is facilitated by contact among workers throughout the hive. Previous studies have shown that the developmental fate of honey bee queens is highly plastic, with queens raised from younger worker larvae exhibiting higher measures of reproductive potential compared to queens raised from older worker larvae. We investigated differences in the chemical composition of the mandibular glands and attractiveness to workers of “high-quality” queens (i.e., raised from first instar worker larvae; more queen-like) and “low-quality” queens (i.e., raised from third instar worker larvae; more worker-like). We characterized the chemical profiles of the mandibular glands of high-quality queens and low-quality queens using GC-MS and used the worker retinue response as a measure of the attractiveness to workers of high-quality queens vs. low-quality queens. We found that queen quality affected the chemical profiles of mandibular gland contents differently across years, showing significant differences in the production of the queen mandibular pheromone (“QMP”) components HVA and 9-HDA in 2010, but no significant differences of any glandular compound in 2012. We also found that workers were significantly more attracted to high-quality queens than to low-quality queens in 2012, possibly because of increased attractiveness of their mandibular gland chemical profiles. Our results indicate that the age at which honey bee larvae enter the “queen-specific” developmental pathway influences the chemical composition of queen mandibular glands and worker behavior. However, these changes are not consistent across years, suggesting that other external factors may play important roles in modulating queen quality.}, number={6}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Rangel, Juliana and Böröczky, Katalin and Schal, Coby and Tarpy, David R.}, editor={Nascimento, Fabio S.Editor}, year={2016}, month={Jun}, pages={e0156027} }
@article{li-byarlay_huang_simone-finstrom_strand_tarpy_rueppell_2016, title={Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage}, volume={83}, ISSN={["1873-6815"]}, DOI={10.1016/j.exger.2016.07.003}, abstractNote={Oxidative stress can lead to premature aging symptoms and cause acute mortality at higher doses in a range of organisms. Oxidative stress resistance and longevity are mechanistically and phenotypically linked; considerable variation in oxidative stress resistance exists among and within species and typically covaries with life expectancy. However, it is unclear whether stress-resistant, long-lived individuals avoid, repair, or tolerate molecular damage to survive longer than others. The honey bee (Apis mellifera L.) is an emerging model system that is well-suited to address this question. Furthermore, this species is the most economically important pollinator, whose health may be compromised by pesticide exposure, including oxidative stressors. Here, we develop a protocol for inducing oxidative stress in honey bee males (drones) via Paraquat injection. After injection, individuals from different colony sources were kept in common social conditions to monitor their survival compared to saline-injected controls. Oxidative stress was measured in susceptible and resistant individuals. Paraquat drastically reduced survival but individuals varied in their resistance to treatment within and among colony sources. Longer-lived individuals exhibited higher levels of lipid peroxidation than individuals dying early. In contrast, the level of protein carbonylation was not significantly different between the two groups. This first study of oxidative stress in male honey bees suggests that survival of an acute oxidative stressor is due to tolerance, not prevention or repair, of oxidative damage to lipids. It also demonstrates colony differences in oxidative stress resistance that might be useful for breeding stress-resistant honey bees.}, journal={EXPERIMENTAL GERONTOLOGY}, author={Li-Byarlay, Hongmei and Huang, Ming Hua and Simone-Finstrom, Michael and Strand, Micheline K. and Tarpy, David R. and Rueppell, Olav}, year={2016}, month={Oct}, pages={15–21} }
@article{traynor_pettis_tarpy_mullin_frazier_frazier_vanengelsdorp_2016, title={In-hive Pesticide Exposome: Assessing risks to migratory honey bees from in-hive pesticide contamination in the Eastern United States}, volume={6}, ISSN={["2045-2322"]}, DOI={10.1038/srep33207}, abstractNote={AbstractThis study measured part of the in-hive pesticide exposome by analyzing residues from live in-hive bees, stored pollen, and wax in migratory colonies over time and compared exposure to colony health. We summarized the pesticide burden using three different additive methods: (1) the hazard quotient (HQ), an estimate of pesticide exposure risk, (2) the total number of pesticide residues, and (3) the number of relevant residues. Despite being simplistic, these models attempt to summarize potential risk from multiple contaminations in real-world contexts. Colonies performing pollination services were subject to increased pesticide exposure compared to honey-production and holding yards. We found clear links between an increase in the total number of products in wax and colony mortality. In particular, we found that fungicides with particular modes of action increased disproportionally in wax within colonies that died. The occurrence of queen events, a significant risk factor for colony health and productivity, was positively associated with all three proxies of pesticide exposure. While our exposome summation models do not fully capture the complexities of pesticide exposure, they nonetheless help elucidate their risks to colony health. Implementing and improving such models can help identify potential pesticide risks, permitting preventative actions to improve pollinator health.}, journal={SCIENTIFIC REPORTS}, author={Traynor, Kirsten S. and Pettis, Jeffery S. and Tarpy, David R. and Mullin, Christopher A. and Frazier, James L. and Frazier, Maryann and vanEngelsdorp, Dennis}, year={2016}, month={Sep} }
@article{simone-finstrom_li-byarlay_huang_strand_rueppell_tarpy_2016, title={Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees}, volume={6}, DOI={10.1038/srep32023}, abstractNote={AbstractMost pollination in large-scale agriculture is dependent on managed colonies of a single species, the honey bee Apis mellifera. More than 1 million hives are transported to California each year just to pollinate the almonds and bees are trucked across the country for various cropping systems. Concerns have been raised about whether such “migratory management” causes bees undue stress; however to date there have been no longer-term studies rigorously addressing whether migratory management is detrimental to bee health. To address this issue, we conducted field experiments comparing bees from commercial and experimental migratory beekeeping operations to those from stationary colonies to quantify effects on lifespan, colony health and productivity and levels of oxidative damage for individual bees. We detected a significant decrease in lifespan of migratory adult bees relative to stationary bees. We also found that migration affected oxidative stress levels in honey bees, but that food scarcity had an even larger impact; some detrimental effects of migration may be alleviated by a greater abundance of forage. In addition, rearing conditions affect levels of oxidative damage incurred as adults. This is the first comprehensive study on impacts of migratory management on the health and oxidative stress of honey bees.}, journal={Scientific Reports}, author={Simone-Finstrom, M. and Li-Byarlay, H. and Huang, M. H. and Strand, M. K. and Rueppell, O. and Tarpy, David}, year={2016} }
@article{lopez-uribe_sconiers_frank_dunn_tarpy_2016, title={Reduced cellular immune response in social insect lineages}, volume={12}, ISSN={["1744-957X"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84962545223&partnerID=MN8TOARS}, DOI={10.1098/rsbl.2015.0984}, abstractNote={
Social living poses challenges for individual fitness because of the increased risk of disease transmission among conspecifics. Despite this challenge, sociality is an evolutionarily successful lifestyle, occurring in the most abundant and diverse group of organisms on earth—the social insects. Two contrasting hypotheses predict the evolutionary consequences of sociality on immune systems. The social group hypothesis posits that sociality leads to stronger individual immune systems because of the higher risk of disease transmission in social species. By contrast, the relaxed selection hypothesis proposes that social species have evolved behavioural immune defences that lower disease risk within the group, resulting in lower immunity at the individual level. We tested these hypotheses by measuring the encapsulation response in 11 eusocial and non-eusocial insect lineages. We built phylogenetic mixed linear models to investigate the effect of behaviour, colony size and body size on cellular immune response. We found a significantly negative effect of colony size on encapsulation response (Markov chain Monte Carlo generalized linear mixed model (mcmcGLMM)
p
<
0.05; phylogenetic generalized least squares (PGLS)
p
<
0.05). Our findings suggest that insects living in large societies may rely more on behavioural mechanisms, such as hygienic behaviours, than on immune function to reduce the risk of disease transmission among nest-mates.
}, number={3}, journal={BIOLOGY LETTERS}, author={Lopez-Uribe, Margarita M. and Sconiers, Warren B. and Frank, Steven D. and Dunn, Robert R. and Tarpy, David R.}, year={2016}, month={Mar} }
@article{lee_steinhauer_rennich_wilson_tarpy_caron_rose_delaplane_baylis_lengerich_et al._2015, title={A national survey of managed honey bee 2013–2014 annual colony losses in the USA}, volume={46}, ISSN={0044-8435 1297-9678}, url={http://dx.doi.org/10.1007/S13592-015-0356-Z}, DOI={10.1007/S13592-015-0356-Z}, abstractNote={Honey bee colony losses are a major concern in the USA and across the globe. Long-term data on losses are critical for putting yearly losses in context. US colony loss surveys have been conducted yearly since the winter of 2006–2007. Here, we report the results from the eighth annual survey on winter losses and the second annual survey of summer and annual losses. There were 7425 valid respondents (7123 backyard, 190 sideline, and 112 commercial beekeepers) managing 497,855 colonies, 19 % of the total US colonies. Total losses reported were 19.8 % [95 % CI 19.3–20.3 %] over the summer, 23.7 % [95 % CI 23.3–24.1 %] over the winter, and 34.1 % [95 % CI 33.6–34.6 %] for the whole year. Average losses were 15.1 % [95 % CI 14.5–15.7 %] over the summer, 44.8 % [95 % CI 43.9–45.7 %] over the winter, and 51.1 % [95 % CI 50.2–51.6 %] for the whole year. While total winter loss was one of the lowest reported in 8 years, 66 % of all beekeepers had higher losses than they deemed acceptable.}, number={3}, journal={Apidologie}, publisher={Springer Science and Business Media LLC}, author={Lee, Kathleen V. and Steinhauer, Nathalie and Rennich, Karen and Wilson, Michael E. and Tarpy, David R. and Caron, Dewey M. and Rose, Robyn and Delaplane, Keith S. and Baylis, Kathy and Lengerich, Eugene J. and et al.}, year={2015}, month={Apr}, pages={292–305} }
@article{seitz_traynor_steinhauer_rennich_wilson_ellis_rose_tarpy_sagili_caron_et al._2015, title={A national survey of managed honey bee 2014–2015 annual colony losses in the USA}, volume={54}, ISSN={0021-8839 2078-6913}, url={http://dx.doi.org/10.1080/00218839.2016.1153294}, DOI={10.1080/00218839.2016.1153294}, abstractNote={Honey bee colony losses are a major concern in the USA and across the globe. Long-term data on losses are critical for putting yearly losses in context. US colony loss surveys have been conducted yearly since the winter of 2006–2007. Here, we report the results from the eighth annual survey on winter losses and the second annual survey of summer and annual losses. There were 7425 valid respondents (7123 backyard, 190 sideline, and 112 commercial beekeepers) managing 497,855 colonies, 19 % of the total US colonies. Total losses reported were 19.8 % [95 % CI 19.3–20.3 %] over the summer, 23.7 % [95 % CI 23.3–24.1 %] over the winter, and 34.1 % [95 % CI 33.6–34.6 %] for the whole year. Average losses were 15.1 % [95 % CI 14.5–15.7 %] over the summer, 44.8 % [95 % CI 43.9–45.7 %] over the winter, and 51.1 % [95 % CI 50.2–51.6 %] for the whole year. While total winter loss was one of the lowest reported in 8 years, 66 % of all beekeepers had higher losses than they deemed acceptable.}, number={4}, journal={Journal of Apicultural Research}, publisher={Informa UK Limited}, author={Seitz, Nicola and Traynor, Kirsten S. and Steinhauer, Nathalie and Rennich, Karen and Wilson, Michael E. and Ellis, James D. and Rose, Robyn and Tarpy, David R. and Sagili, Ramesh R. and Caron, Dewey M. and et al.}, year={2015}, month={Aug}, pages={292–304} }
@article{seeley_tarpy_griffin_carcione_delaney_2015, title={A survivor population of wild colonies of European honeybees in the northeastern United States: investigating its genetic structure}, volume={46}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-015-0355-0}, abstractNote={There is a widespread belief that wild colonies of European honeybees have been eradicated in Europe and North America, killed by viruses spread by the introduced ectoparasitic mite, Varroa destructor. In reality, however, several populations of wild colonies of honeybees in Europe and North America are persisting despite exposure to Varroa. To help understand how this is happening, we tested whether the bees in one of these populations of wild colonies—those living in and around the Arnot Forest (NY, USA)—are genetically distinct from the bees in the nearest managed colonies. We found that the Arnot Forest honeybees are genetically distinct from the honeybees in the two apiaries within 6 km of the forest. Evidently, the population of Arnot Forest honeybees is not supported by a heavy influx of swarms from the nearest managed colonies, which implies that it is self-sustaining. These results suggest that if a closed population of honeybee colonies is allowed to live naturally, it will develop a balanced relationship with its agents of disease. Indeed, it is likely to become well adapted to its local environment as a whole. We suggest four ways to modify beekeeping practices to help honeybees live in greater health.}, number={5}, journal={APIDOLOGIE}, author={Seeley, Thomas D. and Tarpy, David R. and Griffin, Sean R. and Carcione, Angela and Delaney, Deborah A.}, year={2015}, month={Sep}, pages={654–666} }
@article{tarpy_mattila_newton_2015, title={Development of the Honey Bee Gut Microbiome throughout the Queen-Rearing Process}, volume={81}, ISSN={["1098-5336"]}, DOI={10.1128/aem.00307-15}, abstractNote={ABSTRACT
The European honey bee (
Apis mellifera
) is used extensively to produce hive products and for crop pollination, but pervasive concerns about colony health and population decline have sparked an interest in the microbial communities that are associated with these important insects. Currently, only the microbiome of workers has been characterized, while little to nothing is known about the bacterial communities that are associated with queens, even though their health and proper function are central to colony productivity. Here, we provide a large-scale analysis of the gut microbiome of honey bee queens during their developmental trajectory and through the multiple colonies that host them as part of modern queen-rearing practices. We found that queen microbiomes underwent a dramatic shift in size and composition as they aged and encountered different worker populations and colony environments. Queen microbiomes were dominated by enteric bacteria in early life but were comprised primarily of alphaproteobacteria at maturity. Furthermore, queen gut microbiomes did not reflect those of the workers who tended them and, indeed, they lacked many of the bacteria that are considered vital to workers. While worker gut microbiotas were consistent across the unrelated colony populations sampled, the microbiotas of the related queens were highly variable. Bacterial communities in mature queen guts were similar in size to those of mature workers and were characterized by dominant and specific alphaproteobacterial strains known to be associated with worker hypopharyngeal glands. Our results suggest a model in which queen guts are colonized by bacteria from workers' glands, in contrast to routes of maternal inoculation for other animal microbiomes.
}, number={9}, journal={APPLIED AND ENVIRONMENTAL MICROBIOLOGY}, author={Tarpy, David R. and Mattila, Heather R. and Newton, Irene L. G.}, year={2015}, month={May}, pages={3182–3191} }
@article{tarpy_simone-finstrom_linksvayer_2016, title={Honey bee colonies regulate queen reproductive traits by controlling which queens survive to adulthood}, volume={63}, ISSN={["1420-9098"]}, DOI={10.1007/s00040-015-0452-0}, number={1}, journal={INSECTES SOCIAUX}, author={Tarpy, D. R. and Simone-Finstrom, M. and Linksvayer, T. A.}, year={2016}, month={Feb}, pages={169–174} }
@article{tarpy_delaney_seeley_2015, title={Mating Frequencies of Honey Bee Queens (Apis mellifera L.) in a Population of Feral Colonies in the Northeastern United States}, volume={10}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0118734}, abstractNote={Across their introduced range in North America, populations of feral honey bee (Apis mellifera L.) colonies have supposedly declined in recent decades as a result of exotic parasites, most notably the ectoparasitic mite Varroa destructor. Nonetheless, recent studies have documented several wild populations of colonies that have persisted. The extreme polyandry of honey bee queens—and the increased intracolony genetic diversity it confers—has been attributed, in part, to improved disease resistance and may be a factor in the survival of these populations of feral colonies. We estimated the mating frequencies of queens in feral colonies in the Arnot Forest in New York State to determine if the level of polyandry of these queens is especially high and so might contribute to their survival success. We genotyped the worker offspring from 10 feral colonies in the Arnot Forest of upstate New York, as well as those from 20 managed colonies closest to this forest. We found no significant differences in mean mating frequency between the feral and managed queens, suggesting that queens in the remote, low-density population of colonies in the Arnot Forest are neither mate-limited nor adapted to mate at an especially high frequency. These findings support the hypothesis that the hyperpolyandry of honey bees has been shaped on an evolutionary timescale rather than on an ecological one.}, number={3}, journal={PLOS ONE}, author={Tarpy, David R. and Delaney, Deborah A. and Seeley, Thomas D.}, year={2015}, month={Mar} }
@article{rangel_tarpy_2015, title={The combined effects of miticides on the mating health of honey bee (Apis mellifera L.) queens}, volume={54}, ISSN={["2078-6913"]}, DOI={10.1080/00218839.2016.1147218}, abstractNote={The honey bee, Apis mellifera L., plays a pivotal role in the US economy, contributing an estimated $17 billion annually, primarily through crop pollination. Despite their importance, the number of managed honey bee colonies available for pollination services has dropped dramatically during the last decade, threatening crop yields across the country. One of the main culprits of such declines is the varroa mite, Varroa destructor, a pest of honey bees that, when present in high numbers inside a hive, causes colonies to collapse and die. For almost 20 years, varroa mites have been controlled primarily with two in-hive miticides: the pyrethroid tau-fluvalinate (Apistan) and the organophosphate coumaphos (Checkmite+). Various studies have revealed that the exposure of honey bee colonies to sublethal levels of these chemicals can lead to colony-wide health problems. In this study, we looked at the combined effects of fluvalinate and coumaphos on the reproductive health of honey bee queens. We did so by raising queens in either miticide-free beeswax or beeswax containing known concentrations of both coumaphos and fluvalinate. Upon their emergence and successful mating, we took several standard measures of queen’s reproductive health. We found that queens reared in miticide-laden beeswax were not significantly smaller in size, but the spermatheca analysis showed significantly lower sperm counts and viability, and higher mating frequency, compared to queens reared in miticide-free beeswax. Our results indicate that exposure to miticides during development severely compromises queen’s reproductive health. Our findings also demonstrate the importance of the potentially detrimental combined effects of common in-hive miticides on colony health.}, number={3}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Rangel, Juliana and Tarpy, David R.}, year={2015}, pages={275–283} }
@article{youngsteadt_appler_lopez-uribe_tarpy_frank_2015, title={Urbanization Increases Pathogen Pressure on Feral and Managed Honey Bees}, volume={10}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0142031}, abstractNote={Given the role of infectious disease in global pollinator decline, there is a need to understand factors that shape pathogen susceptibility and transmission in bees. Here we ask how urbanization affects the immune response and pathogen load of feral and managed colonies of honey bees (Apis mellifera Linnaeus), the predominant economically important pollinator worldwide. Using quantitative real-time PCR, we measured expression of 4 immune genes and relative abundance of 10 honey bee pathogens. We also measured worker survival in a laboratory bioassay. We found that pathogen pressure on honey bees increased with urbanization and management, and the probability of worker survival declined 3-fold along our urbanization gradient. The effect of management on pathogens appears to be mediated by immunity, with feral bees expressing immune genes at nearly twice the levels of managed bees following an immune challenge. The effect of urbanization, however, was not linked with immunity; instead, urbanization may favor viability and transmission of some disease agents. Feral colonies, with lower disease burdens and stronger immune responses, may illuminate ways to improve honey bee management. The previously unexamined effects of urbanization on honey-bee disease are concerning, suggesting that urban areas may favor problematic diseases of pollinators.}, number={11}, journal={PLOS ONE}, author={Youngsteadt, Elsa and Appler, R. Holden and Lopez-Uribe, Margarita M. and Tarpy, David R. and Frank, Steven D.}, year={2015}, month={Nov} }
@article{steinhauer_rennich_wilson_caron_lengerich_pettis_rose_skinner_tarpy_wilkes_et al._2014, title={A national survey of managed honey bee 2012-2013 annual colony losses in the USA: results from the Bee Informed Partnership}, volume={53}, ISSN={["2078-6913"]}, DOI={10.3896/ibra.1.53.1.01}, abstractNote={Summary For the past six years in which overwintering mortality of honey bee colonies has been surveyed in the USA, estimates of colony loss have fluctuated around one-third of the national population. Here we report on the losses for the 2012–2013 seasons. We collected data from 6,482 US beekeepers (6,114 backyard, 233 sideline, and 135 commercial beekeepers) to document overwintering mortality rates of honey bee colonies for the USA. Responding beekeepers reported a total 30.6% (95% CI: 30.16–31.13%) loss of US colonies over the winter, with each beekeeper losing on average 44.8% (95% CI: 43.88–45.66%) of their colonies. Total winter losses varied across states (range: 11.0% to 54.7%). The self-reported level of acceptable winter loss was 14.6%, and 73.2% of the respondents had mortality rates greater than this level. The leading self-identified causes of overwintering mortality were different according to the operation type; backyard beekeepers generally self-identified “manageable” factors (e.g., starvation, weak colony in the fall), while commercial beekeepers generally identified non-manageable factors (e.g., queen failure, pesticides) as the main cause of losses. For the first time in this series of surveys, we estimated mortality during the summer (total loss = 25.3% (95% CI: 24.80–25.74%), average loss = 12.5% (95% CI: 11.92–13.06%)). The entire 12-months period between April 2012 and April 2013 yielded a total loss of 45.2% (95% CI: 44.58–45.75%), and an average loss of 49.4% (95% CI: 48.46–50.43%). While we found that commercial beekeepers lost fewer colonies than backyard beekeepers in the winter (30.2% (95% CI: 26.54–33.93% vs 45.4% (44.46–46.32%) respectively), the situation was reversed in the summer where commercial beekeepers reported higher average losses than backyard beekeepers (21.6% (95% CI: 18.4–24.79%) vs 12.1% (11.46–12.65%)). These findings demonstrate the ongoing difficulties of US beekeepers in maintaining overall colony heath and survival.}, number={1}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Steinhauer, Nathalie A. and Rennich, Karen and Wilson, Michael E. and Caron, Dewey M. and Lengerich, Eugene J. and Pettis, Jeff S. and Rose, Robyn and Skinner, John A. and Tarpy, David R. and Wilkes, James T. and et al.}, year={2014}, pages={1–18} }
@article{rogers_tarpy_burrack_2014, title={Bee Species Diversity Enhances Productivity and Stability in a Perennial Crop}, volume={9}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0097307}, abstractNote={Wild bees provide important pollination services to agroecoystems, but the mechanisms which underlie their contribution to ecosystem functioning—and, therefore, their importance in maintaining and enhancing these services—remain unclear. We evaluated several mechanisms through which wild bees contribute to crop productivity, the stability of pollinator visitation, and the efficiency of individual pollinators in a highly bee-pollination dependent plant, highbush blueberry. We surveyed the bee community (through transect sampling and pan trapping) and measured pollination of both open- and singly-visited flowers. We found that the abundance of managed honey bees, Apis mellifera, and wild-bee richness were equally important in describing resulting open pollination. Wild-bee richness was a better predictor of pollination than wild-bee abundance. We also found evidence suggesting pollinator visitation (and subsequent pollination) are stabilized through the differential response of bee taxa to weather (i.e., response diversity). Variation in the individual visit efficiency of A. mellifera and the southeastern blueberry bee, Habropoda laboriosa, a wild specialist, was not associated with changes in the pollinator community. Our findings add to a growing literature that diverse pollinator communities provide more stable and productive ecosystem services.}, number={5}, journal={PLOS ONE}, author={Rogers, Shelley R. and Tarpy, David R. and Burrack, Hannah J.}, year={2014}, month={May} }
@article{milbrath_tran_huang_solter_tarpy_lawrence_huang_2015, title={Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera)}, volume={125}, ISSN={["1096-0805"]}, DOI={10.1016/j.jip.2014.12.006}, abstractNote={Honey bees (Apis mellifera) are infected by two species of microsporidia: Nosema apis and Nosema ceranae. Epidemiological evidence indicates that N. ceranae may be replacing N. apis globally in A. mellifera populations, suggesting a potential competitive advantage of N. ceranae. Mixed infections of the two species occur, and little is known about the interactions among the host and the two pathogens that have allowed N. ceranae to become dominant in most geographical areas. We demonstrated that mixed Nosema species infections negatively affected honey bee survival (median survival = 15–17 days) more than single species infections (median survival = 21 days and 20 days for N. apis and N. ceranae, respectively), with median survival of control bees of 27 days. We found similar rates of infection (percentage of bees with active infections after inoculation) for both species in mixed infections, with N. apis having a slightly higher rate (91% compared to 86% for N. ceranae). We observed slightly higher spore counts in bees infected with N. ceranae than in bees infected with N. apis in single microsporidia infections, especially at the midpoint of infection (day 10). Bees with mixed infections of both species had higher spore counts than bees with single infections, but spore counts in mixed infections were highly variable. We did not see a competitive advantage for N. ceranae in mixed infections; N. apis spore counts were either higher or counts were similar for both species and more N. apis spores were produced in 62% of bees inoculated with equal dosages of the two microsporidian species. N. ceranae does not, therefore, appear to have a strong within-host advantage for either infectivity or spore growth, suggesting that direct competition in these worker bee mid-guts is not responsible for its apparent replacement of N. apis.}, journal={JOURNAL OF INVERTEBRATE PATHOLOGY}, author={Milbrath, Meghan O. and Tran, Toan and Huang, Wei-Fong and Solter, Leellen F. and Tarpy, David R. and Lawrence, Frank and Huang, Zachary Y.}, year={2015}, month={Feb}, pages={9–15} }
@article{simone-finstrom_foo_tarpy_starks_2014, title={Impact of Food Availability, Pathogen Exposure, and Genetic Diversity on Thermoregulation in Honey Bees (Apis mellifera)}, volume={27}, ISSN={["1572-8889"]}, DOI={10.1007/s10905-014-9447-3}, number={4}, journal={JOURNAL OF INSECT BEHAVIOR}, author={Simone-Finstrom, M. and Foo, B. and Tarpy, D. R. and Starks, P. T.}, year={2014}, month={Jul}, pages={527–539} }
@article{tarpy_olivarez_2014, title={Measuring sperm viability over time in honey bee queens to determine patterns in stored-sperm and queen longevity}, volume={53}, ISSN={["2078-6913"]}, DOI={10.3896/ibra.1.53.4.02}, abstractNote={Click to increase image sizeClick to decrease image sizeKeywords: queen longevitysupersedurespermathecastored spermsperm viabilitymating quality}, number={4}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Tarpy, David R. and Olivarez, Ray, Jr.}, year={2014}, pages={493–495} }
@article{tarpy_schneider_2014, title={Mechanisms of social evolution: linking adaptative function with proximate mechanisms}, volume={45}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-014-0282-5}, number={3}, journal={APIDOLOGIE}, author={Tarpy, David R. and Schneider, Stanley S.}, year={2014}, month={May}, pages={285–288} }
@article{nino_malka_hefetz_tarpy_grozinger_2013, title={Chemical Profiles of Two Pheromone Glands Are Differentially Regulated by Distinct Mating Factors in Honey Bee Queens (Apis mellifera L.)}, volume={8}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0078637}, abstractNote={Pheromones mediate social interactions among individuals in a wide variety of species, from yeast to mammals. In social insects such as honey bees, pheromone communication systems can be extraordinarily complex and serve to coordinate behaviors among many individuals. One of the primary mediators of social behavior and organization in honey bee colonies is queen pheromone, which is produced by multiple glands. The types and quantities of chemicals produced differ significantly between virgin and mated queens, and recent studies have suggested that, in newly mated queens, insemination volume or quantity can affect pheromone production. Here, we examine the long-term impact of different factors involved during queen insemination on the chemical composition of the mandibular and Dufour's glands, two of the major sources of queen pheromone. Our results demonstrate that carbon dioxide (an anesthetic used in instrumental insemination), physical manipulation of genital tract (presumably mimicking the act of copulation), insemination substance (saline vs. semen), and insemination volume (1 vs. 8 µl) all have long-term effects on mandibular gland chemical profiles. In contrast, Dufour's gland chemical profiles were changed only upon insemination and were not influenced by exposure to carbon dioxide, manipulation, insemination substance or volume. These results suggest that the chemical contents of these two glands are regulated by different neuro-physiological mechanisms. Furthermore, workers responded differently to the different mandibular gland extracts in a choice assay. Although these studies must be validated in naturally mated queens of varying mating quality, our results suggest that while the chemical composition of Dufour's gland is associated with mating status, that of the mandibular glands is associated with both mating status and insemination success. Thus, the queen appears to be signaling both status and reproductive quality to the workers, which may impact worker behavior and physiology as well as social organization and productivity of the colony.}, number={11}, journal={PLOS ONE}, author={Nino, Elina L. and Malka, Osnat and Hefetz, Abraham and Tarpy, David R. and Grozinger, Christina M.}, year={2013}, month={Nov} }
@article{nino_tarpy_grozinger_2013, title={Differential effects of insemination volume and substance on reproductive changes in honey bee queens (Apis mellifera L.)}, volume={22}, ISSN={["1365-2583"]}, DOI={10.1111/imb.12016}, abstractNote={AbstractMating causes dramatic changes in female insects at the behavioural, physiological and molecular level. The factors driving these changes (e.g. seminal proteins, seminal volume) and the molecular pathways by which these factors are operating have been characterized only in a handful of insect species. In the present study, we use instrumental insemination of honey bee queens to examine the role of the insemination substance and volume in triggering post‐mating changes. We also examine differences in gene expression patterns in the fat bodies of queens with highly activated ovaries to determine if events during copulation can cause long‐term changes in gene expression. We found that the instrumental insemination procedure alone caused cessation of mating flights and triggered ovary activation, with high‐volume inseminated queens having the greatest ovary activation. Hierarchical clustering grouped queens primarily by insemination substance and then insemination volume, suggesting that while volume may trigger short‐term physiological changes (i.e. ovary activation) substance plays a greater role in regulating long‐term transcriptional changes. The results of gene ontology analysis and comparison with previous studies suggest that both insemination substance and volume trigger molecular post‐mating changes by altering overlapping gene pathways involved in honey bee reproduction. We also discuss the effects on two genes (vitellogenin and transferrin) involved in reproduction and defence responses.}, number={3}, journal={INSECT MOLECULAR BIOLOGY}, author={Nino, E. L. and Tarpy, D. R. and Grozinger, C. M.}, year={2013}, month={Jun}, pages={233–244} }
@article{tarpy_vanengelsdorp_pettis_2013, title={Genetic diversity affects colony survivorship in commercial honey bee colonies}, volume={100}, ISSN={["1432-1904"]}, DOI={10.1007/s00114-013-1065-y}, abstractNote={Honey bee (Apis mellifera) queens mate with unusually high numbers of males (average of approximately 12 drones), although there is much variation among queens. One main consequence of such extreme polyandry is an increased diversity of worker genotypes within a colony, which has been shown empirically to confer significant adaptive advantages that result in higher colony productivity and survival. Moreover, honey bees are the primary insect pollinators used in modern commercial production agriculture, and their populations have been in decline worldwide. Here, we compare the mating frequencies of queens, and therefore, intracolony genetic diversity, in three commercial beekeeping operations to determine how they correlate with various measures of colony health and productivity, particularly the likelihood of queen supersedure and colony survival in functional, intensively managed beehives. We found the average effective paternity frequency (m e ) of this population of honey bee queens to be 13.6 ± 6.76, which was not significantly different between colonies that superseded their queen and those that did not. However, colonies that were less genetically diverse (headed by queens with m e ≤ 7.0) were 2.86 times more likely to die by the end of the study when compared to colonies that were more genetically diverse (headed by queens with m e > 7.0). The stark contrast in colony survival based on increased genetic diversity suggests that there are important tangible benefits of increased queen mating number in managed honey bees, although the exact mechanism(s) that govern these benefits have not been fully elucidated.}, number={8}, journal={NATURWISSENSCHAFTEN}, author={Tarpy, David R. and vanEngelsdorp, Dennis and Pettis, Jeffrey S.}, year={2013}, month={Aug}, pages={723–728} }
@article{rogers_cajamarca_tarpy_burrack_2013, title={Honey bees and bumble bees respond differently to inter- and intra-specific encounters}, volume={44}, ISSN={["1297-9678"]}, DOI={10.1007/s13592-013-0210-0}, abstractNote={Multiple bee species may forage simultaneously at a common resource. Physical encounters among these bees may modify their subsequent foraging behavior and shape pollinator distribution and resource utilization in a plant community. We observed physical encounters between honey bees, Apis mellifera, and bumble bees, Bombus impatiens, visiting artificial plants in a controlled foraging arena. Both species were more likely to leave the plant following an encounter with another bee, but differed in their responses to intra- and inter-specific encounters. A. mellifera responded similarly to an encounter with either species. However, most B. impatiens that encountered A. mellifera discontinued foraging at the observed plant, but exhibited only a slight decrease in foraging following an intraspecific encounter. Interactions between bees that elicit changes in foraging behavior may have important implications for the pollination of wild and managed plants.}, number={6}, journal={APIDOLOGIE}, author={Rogers, Shelley R. and Cajamarca, Peter and Tarpy, David R. and Burrack, Hannah J.}, year={2013}, month={Nov}, pages={621–629} }
@article{boncristiani_evans_chen_pettis_murphy_lopez_simone-finstrom_strand_tarpy_rueppell_2013, title={In Vitro Infection of Pupae with Israeli Acute Paralysis Virus Suggests Disturbance of Transcriptional Homeostasis in Honey Bees (Apis mellifera)}, volume={8}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0073429}, abstractNote={The ongoing decline of honey bee health worldwide is a serious economic and ecological concern. One major contributor to the decline are pathogens, including several honey bee viruses. However, information is limited on the biology of bee viruses and molecular interactions with their hosts. An experimental protocol to test these systems was developed, using injections of Israeli Acute Paralysis Virus (IAPV) into honey bee pupae reared ex-situ under laboratory conditions. The infected pupae developed pronounced but variable patterns of disease. Symptoms varied from complete cessation of development with no visual evidence of disease to rapid darkening of a part or the entire body. Considerable differences in IAPV titer dynamics were observed, suggesting significant variation in resistance to IAPV among and possibly within honey bee colonies. Thus, selective breeding for virus resistance should be possible. Gene expression analyses of three separate experiments suggest IAPV disruption of transcriptional homeostasis of several fundamental cellular functions, including an up-regulation of the ribosomal biogenesis pathway. These results provide first insights into the mechanisms of IAPV pathogenicity. They mirror a transcriptional survey of honey bees afflicted with Colony Collapse Disorder and thus support the hypothesis that viruses play a critical role in declining honey bee health.}, number={9}, journal={PLOS ONE}, author={Boncristiani, Humberto F. and Evans, Jay D. and Chen, Yanping and Pettis, Jeff and Murphy, Charles and Lopez, Dawn L. and Simone-Finstrom, Michael and Strand, Micheline and Tarpy, David R. and Rueppell, Olav}, year={2013}, month={Sep} }
@article{rogers_tarpy_burrack_2013, title={Multiple Criteria for Evaluating Pollinator Performance in Highbush Blueberry (Ericales: Ericaceae) Agroecosystems}, volume={42}, ISSN={["1938-2936"]}, DOI={10.1603/en12303}, abstractNote={ABSTRACT
Numerous bee species provide pollination services in agricultural ecosystems. Evaluating a pollinator's performance with regard to a crop is an important step in attributing pollination services and predicting how changes in a bee community or foraging environment will affect those services. We used multiple criteria to evaluate pollinators of North Carolina highbush blueberry, Vaccinium corymbosum L., agroecosystems. For five groups of bees (Apis mellifera L., Bombus spp., Habropoda laboriosa F., small native bees, and Xylocopa virginica L.), we measured forager abundance through transect observations, quantified per-visit efficiency as viable seed set resulting from a single visit, and analyzed bee presence in different weather conditions.Wealso considered two other criteria affecting pollinator performance—visitation rate and interspecific influence. A. mellifera was the most abundant bee in the majority of our survey sites, yet had low per-visit efficiency and reduced foraging activity in inclement weather. Small native bees were highly efficient pollinators. Their visits resulted in nearly twice as many seeds as A. mellifera or H. laboriosa. Bombus spp., H. laboriosa, and small native bees were more resilient to fluctuations in temperature, wind speed, and solar radiation than A. mellifera. Although nectar-robbing X. virginica contributed to little pollination through direct flower visits, their presence within the crop impacts the behavior and performance of other individuals. Underscoring the importance of evaluating pollinator performance via multiple criteria, our results show that bee groups contribute to pollination in different ways. These differences may provide functional complementarity and stability of pollination services to agricultural systems.}, number={6}, journal={ENVIRONMENTAL ENTOMOLOGY}, author={Rogers, Shelley R. and Tarpy, David. R. and Burrack, Hannah J.}, year={2013}, month={Dec}, pages={1201–1209} }
@misc{cobey_tarpy_woyke_2013, title={Standard methods for instrumental insemination of Apis mellifera queens}, volume={52}, ISSN={["2078-6913"]}, DOI={10.3896/ibra.1.52.4.09}, abstractNote={Summary Honey bee queens are highly polyandrous and mate in flight. Instrumental insemination is an essential tool that provides complete control of honey bee mating for research and breeding purposes. The technique requires specialized equipment to anesthetize and immobilize the queen and to collect and deliver semen from the drones. Semen is harvested from mature drones by hand eversion of the endophallus and collected into a syringe. The queen is placed in a chamber and anesthetized during the procedure of insertion of semen into the oviducts. Queens are introduced into colonies and their performance can equal to that of naturally mated queens, given proper technique and care.}, number={4}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Cobey, Susan W. and Tarpy, David R. and Woyke, Jerzy}, year={2013} }
@article{vanengelsdorp_tarpy_lengerich_pettis_2013, title={Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States}, volume={108}, ISSN={["1873-1716"]}, DOI={10.1016/j.prevetmed.2012.08.004}, abstractNote={Using standard epidemiological methods, this study set out to quantify the risk associated with exposure to easily diagnosed factors on colony mortality and morbidity in three migratory beekeeping operations. Fifty-six percent of all colonies monitored during the 10-month period died. The relative risk (RR) that a colony would die over the short term (∼50 days) was appreciably increased in colonies diagnosed with Idiopathic Brood Disease Syndrome (IBDS), a condition where brood of different ages appear molten on the bottom of cells (RR = 3.2), or with a "queen event" (e.g., evidence of queen replacement or failure; RR = 3.1). We also found that several risk factors—including the incidence of a poor brood pattern, chalkbood (CB), deformed wing virus (DWV), sacbrood virus (SBV), and exceeding the threshold of 5 Varroa mites per 100 bees—were differentially expressed in different beekeeping operations. Further, we found that a diagnosis of several factors were significantly more or less likely to be associated with a simultaneous diagnosis of another risk factor. These finding support the growing consensus that the causes of colony mortality are multiple and interrelated.}, number={2-3}, journal={PREVENTIVE VETERINARY MEDICINE}, author={vanEngelsdorp, Dennis and Tarpy, David R. and Lengerich, Eugene J. and Pettis, Jeffery S.}, year={2013}, month={Feb}, pages={225–233} }
@article{cornman_tarpy_chen_jeffreys_lopez_pettis_vanengelsdorp_evans_2012, title={Pathogen Webs in Collapsing Honey Bee Colonies}, volume={7}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0043562}, abstractNote={Recent losses in honey bee colonies are unusual in their severity, geographical distribution, and, in some cases, failure to present recognized characteristics of known disease. Domesticated honey bees face numerous pests and pathogens, tempting hypotheses that colony collapses arise from exposure to new or resurgent pathogens. Here we explore the incidence and abundance of currently known honey bee pathogens in colonies suffering from Colony Collapse Disorder (CCD), otherwise weak colonies, and strong colonies from across the United States. Although pathogen identities differed between the eastern and western United States, there was a greater incidence and abundance of pathogens in CCD colonies. Pathogen loads were highly covariant in CCD but not control hives, suggesting that CCD colonies rapidly become susceptible to a diverse set of pathogens, or that co-infections can act synergistically to produce the rapid depletion of workers that characterizes the disorder. We also tested workers from a CCD-free apiary to confirm that significant positive correlations among pathogen loads can develop at the level of individual bees and not merely as a secondary effect of CCD. This observation and other recent data highlight pathogen interactions as important components of bee disease. Finally, we used deep RNA sequencing to further characterize microbial diversity in CCD and non-CCD hives. We identified novel strains of the recently described Lake Sinai viruses (LSV) and found evidence of a shift in gut bacterial composition that may be a biomarker of CCD. The results are discussed with respect to host-parasite interactions and other environmental stressors of honey bees.}, number={8}, journal={PLOS ONE}, author={Cornman, R. Scott and Tarpy, David R. and Chen, Yanping and Jeffreys, Lacey and Lopez, Dawn and Pettis, Jeffery S. and vanEngelsdorp, Dennis and Evans, D.}, year={2012}, month={Aug} }
@article{rangel_keller_tarpy_2013, title={The effects of honey bee (Apis mellifera L.) queen reproductive potential on colony growth}, volume={60}, ISSN={["0020-1812"]}, DOI={10.1007/s00040-012-0267-1}, number={1}, journal={INSECTES SOCIAUX}, author={Rangel, J. and Keller, J. J. and Tarpy, D. R.}, year={2013}, month={Feb}, pages={65–73} }
@article{wilson-rich_tarpy_starks_2012, title={Within- and across-colony effects of hyperpolyandry on immune function and body condition in honey bees (Apis mellifera)}, volume={58}, ISSN={["0022-1910"]}, DOI={10.1016/j.jinsphys.2011.12.020}, abstractNote={Honey bees (Apis mellifera) have become a model system for studies on the influence of genetic diversity on disease. Honey bee queens mate with a remarkably high number of males-up to 29 in the current study-from which they produce a colony of genetically diverse daughter workers. Recent evidence suggests a significant benefit of intracolony genetic diversity on disease resistance. Here, we explored the relationship between the level of genetic diversity and multiple physiological mechanisms of cellular and humoral immune defense (encapsulation response and phenoloxidase activity). We also investigated an effect of genetic diversity on a measure of body condition (fat body mass). While we predicted that mean colony phenoloxidase activity, encapsulation response, and fat body mass would show a positive relationship with increased intracolonial genetic diversity, we found no significant relationship between genetic diversity and these immune measures, and found no consistent effect on body condition. These results suggest that high genetic diversity as a result of extreme polyandry may have little bearing on the physiological mechanisms of immune function at naturally occurring mating levels in honey bees.}, number={3}, journal={JOURNAL OF INSECT PHYSIOLOGY}, author={Wilson-Rich, Noah and Tarpy, David R. and Starks, Philip T.}, year={2012}, month={Mar}, pages={402–407} }
@article{richard_schal_tarpy_grozinger_2011, title={Effects of Instrumental Insemination and Insemination Quantity on Dufour’s Gland Chemical Profiles and Vitellogenin Expression in Honey Bee Queens (Apis mellifera)}, volume={37}, ISSN={0098-0331 1573-1561}, url={http://dx.doi.org/10.1007/s10886-011-9999-z}, DOI={10.1007/s10886-011-9999-z}, abstractNote={Honey bee queens (Apis mellifera) mate in their early adult lives with a variable number of males (drones). Mating stimulates dramatic changes in queen behavior, physiology, gene expression, and pheromone production. Here, we used virgin, single drone- (SDI), and multi-drone- (MDI) inseminated queens to study the effects of instrumental insemination and insemination quantity on the pheromone profiles of the Dufour's gland, and the expression of the egg-yolk protein, vitellogenin, in the fat body. Age, environmental conditions, and genetic background of the queens were standardized to specifically characterize the effects of these treatments. Our data demonstrate that insemination and insemination quantity significantly affect the chemical profiles of the Dufour's gland secretion. Moreover, workers were more attracted to Dufour's gland extract from inseminated queens compared to virgins, and to the extract of MDI queens compared to extract of SDI queens. However, while there were differences in the amounts of some esters between MDI queens and the other groups, it appears that the differences in behavioral responses were elicited by subtle changes in the overall chemical profiles rather than dramatic changes in specific individual chemicals. We also found a decrease in vitellogenin gene expression in the fat body of the MDI queens, which is negatively correlated with the quantities of Dufour's gland content. The possible explanations of this reduction are discussed.}, number={9}, journal={Journal of Chemical Ecology}, publisher={Springer Science and Business Media LLC}, author={Richard, Freddie-Jeanne and Schal, Coby and Tarpy, David R. and Grozinger, Christina M.}, year={2011}, month={Jul}, pages={1027–1036} }
@article{tarpy_keller_caren_delaney_2011, title={Experimentally induced variation in the physical reproductive potential and mating success in honey bee queens}, volume={58}, ISSN={["1420-9098"]}, DOI={10.1007/s00040-011-0180-z}, number={4}, journal={INSECTES SOCIAUX}, author={Tarpy, D. R. and Keller, J. J. and Caren, J. R. and Delaney, D. A.}, year={2011}, month={Nov}, pages={569–574} }
@article{nino_tarpy_grozinger_2011, title={Genome-wide analysis of brain transcriptional changes in honey bee (Apis mellifera L.) queens exposed to carbon dioxide and physical manipulation}, volume={20}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2011.2011.01072.x}, abstractNote={Mating is a complex process causing many behavioural and physiological changes, but the factors triggering them and the underlying molecular processes are not well characterized. In the present study we examine the effects of CO2 (a commonly used anaesthetic in instrumental insemination that causes changes similar to those occurring after mating) and physical manipulation (which may mimic certain aspects of copulation) on the behavioural, physiological and brain transcriptional changes in honey bee queens. We show that while CO2 causes cessation of mating flights and ovary activation, physical manipulation has additional effects on ovary activation and brain transcriptional changes. Comparisons with previous studies of honey bees and female Drosophila indicate that common molecular mechanisms may be responsible for regulating reproductive changes across different mating regimes and insect orders.}, number={3}, journal={INSECT MOLECULAR BIOLOGY}, author={Nino, E. L. and Tarpy, D. R. and Grozinger, C.}, year={2011}, month={Jun}, pages={387–398} }
@article{jackson_tarpy_fahrbach_2011, title={Histological estimates of ovariole number in honey bee queens, Apis mellifera, reveal lack of correlation with other queen quality measures}, volume={11}, DOI={10.1673/031.011.8201}, abstractNote={Abstract Published estimates of the number of ovarioles found in the ovaries of honey bee, Apis mellifera L. (Hymenoptera: Apidae) queens range from 100 to 180 per ovary. Within the context of a large-scale study designed to assay the overall quality of queens obtained from various commercial sources, a simple histology-based method for accurate determination of ovariole number was developed and then applied to a sample of 75 queens. Although all 10 commercial sources evaluated provided queens with ovariole numbers within the expected range, ovariole number was found to vary significantly across sources. Overall, and within most of the individual samples, there was no correlation of ovariole number with other morphological attributes such as thoracic width, wing length, or wet weight. Queens from two of the sources, however, displayed a significant negative relationship between wet weight and ovariole number. This study provides baseline data on ovariole number in commercial honey bee queens in the United States at a time when honey bee populations are declining; the method described can be used in studies relating ovariole number in queens to egg production and behavior.}, journal={Journal of Insect Science (Tucson, AZ)}, author={Jackson, J. T. and Tarpy, David and Fahrbach, S. E.}, year={2011} }
@article{williams_tarpy_vanengelsdorp_chauzat_cox-foster_delaplane_neumann_pettis_rogers_shutler_2010, title={Colony Collapse Disorder in context}, volume={32}, ISSN={["1521-1878"]}, DOI={10.1002/bies.201000075}, abstractNote={Although most of humanity relies upon foods that do not require animal pollination 1, production of 39 of the world's 57 most important monoculture crops still benefits from this ecosystem service 2. Western honey bees (Apis mellifera) are undoubtedly the single-most valuable animal pollinators to agriculture because they can be easily maintained and transported to pollinator-dependent crops. Yet, despite an almost 50% increase in world honey bee stocks over the last century, beekeepers have not kept pace with the >300% increase in pollinator-dependent crops 3. This has led to great uncertainty surrounding the recent large-scale die-offs of honey bees around the world, and has sparked enormous interest from both scientists and the general public.}, number={10}, journal={BIOESSAYS}, author={Williams, Geoffrey R. and Tarpy, David R. and vanEngelsdorp, Dennis and Chauzat, Marie-Pierre and Cox-Foster, Diana L. and Delaplane, Keith S. and Neumann, Peter and Pettis, Jeffery S. and Rogers, Richard E. L. and Shutler, Dave}, year={2010}, month={Oct}, pages={845–846} }
@article{tarpy_caren_delaney_sammataro_finley_loper_degrandi-hoffman_2010, title={Mating frequencies of Africanized honey bees in the south western USA}, volume={49}, ISSN={["2078-6913"]}, DOI={10.3896/ibra.1.49.4.02}, abstractNote={Summary Emerging evidence suggests that there are significant adaptive advantages conferred to genetically diverse honey bee colonies through multiple matings with queens. We determined the intracolony genetic diversity of Africanized honey bee (AHB) colonies from a feral population in the south western USA. A total of 1,253 worker offspring were genotyped from 20 feral colonies (all but three of African mitotype), four managed AHB, three managed European honey bee (EHB), and four control colonies (headed by EHB queens instrumentally inseminated with one, two, five, or ten drones, respectively) using eight microsatellite markers. The 17 feral AHB queens mated with an average of 20.0 ± 6.53 (range 10–32) drones, resulting in effective paternity frequencies of 20.0 ± 8.46 (range 10.56–37.53), which is one of the highest mating numbers recorded within the species. Though Africanized honey bee colonies are among the most genetically diverse Apis mellifera yet recorded, their queen mating frequencies are within the expected range of the species overall, including African honey bees in their native range. The factors responsible for these findings are discussed.}, number={4}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Tarpy, David R. and Caren, Joel R. and Delaney, Deborah A. and Sammataro, Diana and Finley, Jennifer and Loper, Gerald M. and DeGrandi-Hoffman, Gloria}, year={2010}, pages={302–310} }
@article{delaney_keller_caren_tarpy_2011, title={The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera L.)}, volume={42}, ISSN={["1297-9678"]}, DOI={10.1051/apido/2010027}, abstractNote={Understanding the reproductive potential (“quality”) of queens bees can provide valuable insights into factors that influence colony phenotype. We assayed queens from various commercial sources for various measures of potential queen quality, including their physical characters (such as their degree of parasitism), insemination number (stored sperm counts), and effective paternity frequency (number of drone fathers among their offspring). We found significant variation in the physical, insemination, and mating quality of commercially produced queens, and we detected significant correlations within and among these various measures. Overall, the queens were sufficiently inseminated (3.99 ± 1.504 million sperm) and mated with an appropriate number of drones (effective paternity frequency: 16.0 ± 9.48). Importantly, very few of the queens were parasitized by tracheal mites and none were found with either Nosema species. These findings suggest possible mechanisms for assessing the potential fitness of honey bee queens without the need for destructive sampling.}, number={1}, journal={APIDOLOGIE}, author={Delaney, Deborah A. and Keller, Jennifer J. and Caren, Joel R. and Tarpy, David R.}, year={2011}, month={Jan}, pages={1–13} }
@article{vanengelsdorp_speybroeck_evans_nguyen_mullin_frazier_frazier_cox-foster_chen_tarpy_et al._2010, title={Weighing Risk Factors Associated With Bee Colony Collapse Disorder by Classification and Regression Tree Analysis}, volume={103}, ISSN={["1938-291X"]}, DOI={10.1603/ec09429}, abstractNote={ABSTRACT Colony collapse disorder (CCD), a syndrome whose defining trait is the rapid loss of adult worker honey bees, Apis mellifera L., is thought to be responsible for a minority of the large overwintering losses experienced by U.S. beekeepers since the winter 2006–2007. Using the same data set developed to perform a monofactorial analysis (PloS ONE 4: e6481, 2009), we conducted a classification and regression tree (CART) analysis in an attempt to better understand the relative importance and interrelations among different risk variables in explaining CCD. Fifty-five exploratory variables were used to construct two CART models: one model with and one model without a cost of misclassifying a CCD-diagnosed colony as a non-CCD colony. The resulting model tree that permitted for misclassification had a sensitivity and specificity of 85 and 74%, respectively. Although factors measuring colony stress (e.g., adult bee physiological measures, such as fluctuating asymmetry or mass of head) were important discriminating values, six of the 19 variables having the greatest discriminatory value were pesticide levels in different hive matrices. Notably, coumaphos levels in brood (a miticide commonly used by beekeepers) had the highest discriminatory value and were highest in control (healthy) colonies. Our CART analysis provides evidence that CCD is probably the result of several factors acting in concert, making afflicted colonies more susceptible to disease. This analysis highlights several areas that warrant further attention, including the effect of sublethal pesticide exposure on pathogen prevalence and the role of variability in bee tolerance to pesticides on colony survivorship.}, number={5}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={vanEngelsdorp, Dennis and Speybroeck, Niko and Evans, Jay D. and Nguyen, Bach Kim and Mullin, Chris and Frazier, Maryann and Frazier, Jim and Cox-Foster, Diana and Chen, Yanping and Tarpy, David R. and et al.}, year={2010}, month={Oct}, pages={1517–1523} }
@article{vanengelsdorp_evans_donovall_mullin_frazier_frazier_tarpy_hayes_pettis_2009, title={"Entombed Pollen": A new condition in honey bee colonies associated with increased risk of colony mortality}, volume={101}, ISSN={["0022-2011"]}, DOI={10.1016/j.jip.2009.03.008}, abstractNote={Here we describe a new phenomenon, entombed pollen, which is highly associated with increased colony mortality. Entombed pollen is sunken, capped cells amidst "normal", uncapped cells of stored pollen, and some of the pollen contained within these cells is brick red in color. There appears to be a lack of microbial agents in the pollen, and larvae and adult bees do not have an increased rate of mortality when they are fed diets supplemented with entombed pollen in vitro, suggesting that the pollen itself is not directly responsible for increased colony mortality. However, the increased incidence of entombed pollen in reused wax comb suggests that there is a transmittable factor common to the phenomenon and colony mortality. In addition, there were elevated pesticide levels, notably of the fungicide chlorothalonil, in entombed pollen. Additional studies are needed to determine if there is a causal relationship between entombed pollen, chemical residues, and colony mortality.}, number={2}, journal={JOURNAL OF INVERTEBRATE PATHOLOGY}, author={vanEngelsdorp, Dennis and Evans, Jay D. and Donovall, Leo and Mullin, Chris and Frazier, Maryann and Frazier, James and Tarpy, David R. and Hayes, Jerry, Jr. and Pettis, Jeffery S.}, year={2009}, month={Jun}, pages={147–149} }
@article{kocher_richard_tarpy_grozinger_2009, title={Queen reproductive state modulates pheromone production and queen-worker interactions in honeybees}, volume={20}, ISSN={["1465-7279"]}, DOI={10.1093/beheco/arp090}, abstractNote={The mandibular glands of queen honeybees produce a pheromone that modulates many aspects of worker honeybee physiology and behavior and is critical for colony social organization. The exact chemical blend produced by the queen differs between virgin and mated, laying queens. Here, we investigate the role of mating and reproductive state on queen pheromone production and worker responses. Virgin queens, naturally mated queens, and queens instrumentally inseminated with either semen or saline were collected 2 days after mating or insemination. Naturally mated queens had the most activated ovaries and the most distinct chemical profile in their mandibular glands. Instrumentally inseminated queens were intermediate between virgins and naturally mated queens for both ovary activation and chemical profiles. There were no significant differences between semen- and saline-inseminated queens. Workers were preferentially attracted to the mandibular gland extracts from queens with significantly more activated ovaries. These studies suggest that the queen pheromone blend is modulated by the reproductive status of the queens, and workers can detect these subtle differences and are more responsive to queens with higher reproductive potential. Furthermore, it appears as if insemination substance does not strongly affect physiological characteristics of honeybee queens 2 days after insemination, suggesting that the insemination process or volume is responsible for stimulating these early postmating changes in honeybee queens.}, number={5}, journal={BEHAVIORAL ECOLOGY}, author={Kocher, Sarah D. and Richard, Freddie-Jeanne and Tarpy, David R. and Grozinger, Christina M.}, year={2009}, pages={1007–1014} }
@article{kocher_tarpy_grozinger_2010, title={The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression}, volume={19}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2009.00965.x}, abstractNote={AbstractMating is fundamental to most organisms, although the physiological and transcriptional changes associated with this process have been largely characterized only in Drosophila melanogaster. In this study, we use honey bees as a model system because their queens undergo massive and permanent physiological and behavioural changes following mating. Previous studies have identified changes associated with the transition from a virgin queen to a fully mated, egg‐laying queen. Here, we further uncouple the mating process to examine the effects of natural mating vs. instrumental insemination and saline vs. semen insemination. We observed effects on flight behaviour, vitellogenin expression and significant overlap in transcriptional profiles between our study and analogous studies in D. melanogaster, suggesting that some post‐mating mechanisms are conserved across insect orders.}, number={2}, journal={INSECT MOLECULAR BIOLOGY}, author={Kocher, S. D. and Tarpy, D. R. and Grozinger, C. M.}, year={2010}, month={Apr}, pages={153–162} }
@article{tarpy_mayer_2009, title={The effects of size and reproductive quality on the outcomes of duels between honey bee queens (Apis mellifera L.)}, volume={21}, ISSN={["1828-7131"]}, DOI={10.1080/08927014.2009.9522503}, abstractNote={Honey bee queens engage in fatal fights during colony reproductive episodes to become the next egg layer of the colony. We investigated if there is an inherent size advantage among competing queens by staging paired duels in artificial fighting arenas. We raised queens of either highor low-reproductive quality and paired queens to maximize the weight difference between them. We found that heavier queens were significantly more likely to survive than lighter queens. Given that heavier queens do not seem to have an advantage in vivo, these results suggest that there may be opposing levels of selection acting on queen duels at the individual and colony levels.}, number={2}, journal={ETHOLOGY ECOLOGY & EVOLUTION}, author={Tarpy, D. R. and Mayer, M. K.}, year={2009}, month={Aug}, pages={147–153} }
@article{kocher_richard_tarpy_grozinger_2008, title={Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera)}, volume={9}, ISSN={["1471-2164"]}, DOI={10.1186/1471-2164-9-232}, abstractNote={Abstract
Background
The molecular mechanisms underlying the post-mating behavioral and physiological transitions undergone by females have not been explored in great detail. Honey bees represent an excellent model system in which to address these questions because they exhibit a range of "mating states," with two extremes (virgins and egg-laying, mated queens) that differ dramatically in their behavior, pheromone profiles, and physiology. We used an incompletely-mated mating-state to understand the molecular processes that underlie the transition from a virgin to a mated, egg-laying queen. We used same-aged virgins, queens that mated once but did not initiate egg-laying, and queens that mated once and initiated egg-laying.
Results
Differences in the behavior and physiology among groups correlated with the underlying variance observed in the top 50 predictive genes in the brains and the ovaries. These changes were correlated with either a behaviorally-associated pattern or a physiologically-associated pattern. Overall, these results suggest that the brains and the ovaries of queens are uncoupled or follow different timescales; the initiation of mating triggers immediate changes in the ovaries, while changes in the brain may require additional stimuli or take a longer time to complete. Comparison of our results to previous studies of post-mating changes in Drosophila melanogaster identified common biological processes affected by mating, including stress response and alternative-splicing pathways. Comparison with microarray data sets related to worker behavior revealed no obvious correlation between genes regulated by mating and genes regulated by behavior/physiology in workers.
Conclusion
Studying the underlying molecular mechanisms of post-mating changes in honey bee queens will not only give us insight into how molecular mechanisms regulate physiological and behavioral changes, but they may also lead to important insights into the evolution of social behavior. Post-mating changes in gene regulation in the brains and ovaries of honey bee queens appear to be triggered by different stimuli and may occur on different timescales, potentially allowing changes in the brains and the ovaries to be uncoupled.
}, journal={BMC GENOMICS}, author={Kocher, Sarah D. and Richard, Freddie-Jeanne and Tarpy, David R. and Grozinger, Christina M.}, year={2008}, month={May} }
@article{tarpy_summers_keller_2007, title={Comparison of parasitic mites in Russian-Hybrid and Italian honey bee (Hymenoptera : Apidae) colonies across three different locations in north Carolina}, volume={100}, ISSN={["0022-0493"]}, DOI={10.1603/0022-0493(2007)100[258:COPMIR]2.0.CO;2}, abstractNote={Abstract The most economically important parasites of honey bee, Apis mellifera L. (Hymenoptera: Apidae), colonies are the parasitic mites Varroa destructor Anderson & Trueman and Acarapis woodi (Rennie). Research has shown that mite-tolerant stocks are effective means to reduce mite infestations within colonies, but it is unclear whether the stocks available commercially are viable means of mite control because they are likely to be genetic hybrids. We compared colonies of a standard commercial stock (“Italian”) with those of a commercially purchased mite-tolerant stock (“Russian”) for their levels of varroa and “tracheal” mites (A. woodi) over the course of 2 yr in three different geographic locations. We were unable to detect significant infestations of tracheal mites; thus, we were unable to adequately compare the stocks for their tolerance. In contrast, we found significant differences in the levels of varroa mites within and among colonies located across the three different study sites for both years. By the end of the first year, we found statistically significant differences between the stocks in varroa mite intensity (mites per adult bee), such that Russian-hybrid colonies tended to have a significantly lower proportion of parasitized adult bees than Italian colonies. In the second year, we found statistically significant differences between the stocks in varroa mite load (daily mite drop), such that Russian-hybrid colonies tended to have lower total numbers of mites than Italian colonies. These findings suggest that beekeepers may benefit by incorporating commercially purchased mite-tolerant stocks into their existing integrated pest management programs.}, number={2}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Tarpy, David R. and Summers, Joshua and Keller, Jennifer J.}, year={2007}, month={Apr}, pages={258–266} }
@article{kreitlow_tarpy_2006, title={Environmental and genotypic effects on Russian-hybrid and Italian honey bee (Apis mellifera) (Hymenoptera : Apidae) foraging behavior}, volume={35}, ISSN={["0046-225X"]}, DOI={10.1603/0046-225X(2006)35[1610:EAGEOR]2.0.CO;2}, abstractNote={Abstract Both environment and genotype have a significant influence on the foraging behavior of honey bees (Apis mellifera). We compared the colony-level foraging behaviors of two honey bee stocks at three different sites by sampling 50 foragers each from 16 Russian-hybrid and 16 Italian colonies distributed among the Coastal Plain, Piedmont, and Mountain regions of North Carolina. We detected highly significant differences in foraging behavior among the different sites, but we found very few differences between the stocks. Moreover, there were very few environment–genotype interactions on foraging behavior, suggesting that the effect of genotype does not vary significantly depending on the environment in which it is located. These findings suggest that, while there are some notable differences between Russian-hybrid and Italian honey bees, the environment has a relatively larger impact on honey bee foraging behavior for these two stocks.}, number={6}, journal={ENVIRONMENTAL ENTOMOLOGY}, author={Kreitlow, K. Lane and Tarpy, David R.}, year={2006}, month={Dec}, pages={1610–1616} }
@article{tarpy_seeley_2006, title={Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens}, volume={93}, ISSN={["1432-1904"]}, DOI={10.1007/s00114-006-0091-4}, abstractNote={We studied the relationship between genetic diversity and disease susceptibility in honeybee colonies living under natural conditions. To do so, we created colonies in which each queen was artificially inseminated with sperm from either one or ten drones. Of the 20 colonies studied, 80% showed at least one brood disease. We found strong differences between the two types of colonies in the infection intensity of chalkbrood and in the total intensity of all brood diseases (chalkbrood, sacbrood, American foulbrood, and European foulbrood) with both variables lower for the colonies with higher genetic diversity. Our findings demonstrate that disease can be an important factor in the ecology of honeybee colonies and they provide strong support for the disease hypothesis for the evolution of polyandry by social insect queens.}, number={4}, journal={NATURWISSENSCHAFTEN}, author={Tarpy, DR and Seeley, TD}, year={2006}, month={Apr}, pages={195–199} }
@article{seeley_tarpy_2007, title={Queen promiscuity lowers disease within honeybee colonies}, volume={274}, ISSN={["1471-2954"]}, DOI={10.1098/rspb.2006.3702}, abstractNote={Most species of social insects have singly mated queens, but in some species each queen mates with numerous males to create a colony with a genetically diverse worker force. The adaptive significance of polyandry by social insect queens remains an evolutionary puzzle. Using the honeybee (Apis mellifera), we tested the hypothesis that polyandry improves a colony's resistance to disease. We established colonies headed by queens that had been artificially inseminated by either one or 10 drones. Later, we inoculated these colonies with spores ofPaenibacillus larvae, the bacterium that causes a highly virulent disease of honeybee larvae (American foulbrood). We found that, on average, colonies headed by multiple-drone inseminated queens had markedly lower disease intensity and higher colony strength at the end of the summer relative to colonies headed by single-drone inseminated queens. These findings support the hypothesis that polyandry by social insect queens is an adaptation to counter disease within their colonies.}, number={1606}, journal={PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES}, author={Seeley, Thomas D. and Tarpy, David R.}, year={2007}, month={Jan}, pages={67–72} }
@article{johnson_zaman_decelle_siegel_tarpy_siegel_starks_2005, title={Multiple micro-organisms in chalkbrood mummies: evidence and implications}, volume={44}, ISSN={["2078-6913"]}, DOI={10.1080/00218839.2005.11101143}, abstractNote={SUMMARY The pathogenic fungus Ascosphaera apis is the causative agent of the brood disease chalkbrood in honey bee (Apis mellifera) larvae. Infected, hardened larvae—in a powdered form—have been used to inoculate experimental honey bee colonies. While attempting to grow a pure isolate of A. apis from chalkbrood infected larvae, we discovered (via Gram staining and sequencing of the 5.8S rDNA region) that the inoculum also harbours many species of bacteria and additional species of fungi. Some of these fungi have been identified previously as antagonists of A. apis. It is not surprising that bacteria and fungi grow on dead bees; however, our data indicate that previous experiments intended to study the effects of A. apis in honey bees have rather studied the response of honey bees to a cocktail of fungal and bacterial agents. Accordingly, our results indicate that previous research on the A. apis-honey bee disease system was not specific to A. apis and raise the possibility that the observed honey bee response may have been muted, magnified, or both.}, number={1}, journal={JOURNAL OF APICULTURAL RESEARCH}, author={Johnson, RN and Zaman, MT and Decelle, MM and Siegel, AJ and Tarpy, DR and Siegel, EC and Starks, PT}, year={2005}, pages={29–32} }
@article{gilley_tarpy_2005, title={Three mechanisms of queen elimination in swarming honey bee colonies}, volume={36}, ISSN={0044-8435 1297-9678}, url={http://dx.doi.org/10.1051/APIDO:2005033}, DOI={10.1051/APIDO:2005033}, abstractNote={L'elimination d'une reine est un processus par lequel toutes les reines non accouplees et produites au cours de la scission (essaimage) de la colonie, sauf une, sont eliminees du nid parental. La figure 1 montre comment l'elimination des reines est liee au processus de scission dans une colonie typique d'abeilles. Les reines sont eliminees selon trois mecanismes : les duels reine-reine. les assassinats de reines et le depart avec l'essaim. Nous passons d'abord en revue ce qui est connu concernant chacun de ces mecanismes d'elimination. Puis nous avons utilise de nouvelles donnees provenant de colonies logees dans des ruches d'observation qui essaimaient et avons en meme temps re-analyse les donnees de la litterature pour repondre a cinq questions sur la biologie de l'elimination des reines, que nous considerons comme remarquables : (1) les roles relatifs des trois mecanismes dans le resultat de l'elimination des reines, (2) le deroulement typique des evenements dans le nid au cours de l'elimination, (3) le role joue par les ouvrieres (4) l'action de « l'aspersion » (par des matieres fecales)sur le resultat de l'elimination, (5) les differences entre les abeilles europeennes (Apis mellifera ligustica) et africaines (A. m. scutellata) dans ce processus. Les tableaux I et II decrivent les evenements qui ont eu lieu au sein des six colonies d'abeilles europeennes et des sept colonies d'abeilles africaines. Le tableau III quantifie le nombre de reines eliminees par chaque mecanisme. La figure 2 montre le deroulement des evenements. La largeur de la fleche represente le nombre de colonies qui suit le deroulement indique. Les cercles noirs et blancs indiquent pour chaque colonie l'etape finale (i.e. la reine restante qui herite du nid), a partir de laquelle on peut remonter la sequence des evenements jusqu'au depart de l'essaim primaire. Nous tirons de nos resultats les conclusions suivantes: (1) les evenements au cours de l'elimination des reines peuvent etre divises en deux series distinctes: les colonies sans duels de reines, d'ou emerge une reine qui assassine toutes ses rivales, et les colonies avec duels de reines, ou une suite tres variable d'evenements se succedent incluant le depart d'au moins un essaim secondaire (Fig. 2); (2) le mecanisme d'elimination le plus commun est le duel, mais la contribution de chaque mecanisme au resultat final depend du deroulement des evenements que suit une colonie; (3) les ouvrieres ne tuent pas les reines et ne les blessent pas serieusement, mais elles interagissent avec les reines de certaines facons qui peuvent etre couteuses pour les reines; (4) l'aspersion dans un contexte naturel aboutit a attirer les ouvrieres sur la reine aspergee; (5) les abeilles europeennes et africaines utilisent les memes mecanismes, mais des differences existent probablement dans la frequence relative de chacun d'entre eux.}, number={3}, journal={Apidologie}, publisher={Springer Science and Business Media LLC}, author={Gilley, David C. and Tarpy, David R.}, year={2005}, month={Jul}, pages={461–474} }
@article{tarpy_nielsen_nielsen_2004, title={A scientific note on the revised estimates of effective paternity frequency in Apis}, volume={51}, ISSN={["1420-9098"]}, DOI={10.1007/s00040-004-0734-4}, number={2}, journal={INSECTES SOCIAUX}, author={Tarpy, DR and Nielsen, R and Nielsen, DI}, year={2004}, month={May}, pages={203–204} }
@misc{tarpy_gilley_2004, title={Group decision making during queen production in colonies of highly eusocial bees}, volume={35}, ISSN={["1297-9678"]}, DOI={10.1051/apido:2004008}, abstractNote={Colonies of social insects make numerous group decisions about foraging, nest maintenance, and reproduction. Queen production is a task whereby a colony's workers may exercise choices over which individuals to rear as gynes (unmated queens) and which gynes will survive to ultimately become queens. Here we assess the potential for how colonies of highly eusocial bees may exhibit such group decisions by reviewing the behaviors of stingless bee and honey bee workers during the gyne rearing, emergence, and elimination stages of queen production. We demonstrate that although the specific mechanisms whereby such decisions are manifested may vary among the taxa, there is a high potential for group decision making during queen production in eusocial bees. Given the importance of a queen to the inclusive fitness of all nestmates, such group decisions are likely to have a profound influence on the reproductive success of highly eusocial bee colonies. We briefly entertain the evolutionary mechanisms that may have shaped these group decision-making processes. queen rearing / group decision making / queen elimination / colony reproduction / highly eusocial bees}, number={2}, journal={APIDOLOGIE}, author={Tarpy, DR and Gilley, DC}, year={2004}, pages={207–216} }
@misc{tarpy_gilley_seeley_2004, title={Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement}, volume={55}, ISSN={["1432-0762"]}, DOI={10.1007/s00265-003-0738-5}, number={6}, journal={BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY}, author={Tarpy, DR and Gilley, DC and Seeley, TD}, year={2004}, month={Apr}, pages={513–523} }
@article{tarpy_2003, title={Bet hedging by honey bee queens}, volume={143}, number={12}, journal={American Bee Journal}, author={Tarpy, D.}, year={2003}, month={Dec}, pages={937–939} }
@article{lee_steinhauer_rennich_wilson_tarpy_caron_rose_delaplane_baylis_lengerich_et al., title={A national survey of managed honey bee 2013-2014 annual colony losses in the USA}, volume={46}, number={3}, journal={Apidologie}, author={Lee, K. V. and Steinhauer, N. and Rennich, K. and Wilson, M. E. and Tarpy, D. R. and Caron, D. M. and Rose, R. and Delaplane, K. S. and Baylis, K. and Lengerich, E. J. and et al.}, pages={292–305} }
@article{seitz_traynor_steinhauer_rennich_wilson_ellis_rose_tarpy_sagili_caron_et al., title={A national survey of managed honey bee 2014-2015 annual colony losses in the USA}, volume={54}, number={4}, journal={Journal of Apicultural Research}, author={Seitz, N. and Traynor, K. S. and Steinhauer, N. and Rennich, K. and Wilson, M. E. and Ellis, J. D. and Rose, R. and Tarpy, D. R. and Sagili, R. R. and Caron, D. M. and et al.}, pages={292–304} }
@article{tarpy_summers_keller_hensey, title={Comparing pairs of Russian and Italian colonies by new beekeepers in North Carolina}, volume={147}, number={2}, journal={American Bee Journal}, author={Tarpy, D. R. and Summers, J. and Keller, J. J. and Hensey, W.}, pages={149–152} }
@misc{human_brodschneider_dietemann_dively_ellis_forsgren_fries_hatjina_hu_jaffe_et al., title={Miscellaneous standard methods for Apis mellifera research}, volume={52}, number={4}, journal={Journal of Apicultural Research}, author={Human, H. and Brodschneider, R. and Dietemann, V. and Dively, G. and Ellis, J. D. and Forsgren, E. and Fries, I. and Hatjina, F. and Hu, F. L. and Jaffe, R. and et al.} }