@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={Drone 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{mcafee_stillman_marshall_metz_2022, title={Editorial: Insect Fertility in a Changing Environment}, volume={10}, ISSN={["2296-701X"]}, DOI={10.3389/fevo.2022.847997}, abstractNote={EDITORIAL article Front. Ecol. Evol., 11 February 2022 | https://doi.org/10.3389/fevo.2022.847997}, journal={FRONTIERS IN ECOLOGY AND EVOLUTION}, author={McAfee, Alison and Stillman, Jonathon H. and Marshall, Katie E. and Metz, Bradley N.}, year={2022}, month={Feb} }
 @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={Abstract Declining 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{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={Honey 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{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{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={Abstract Queens 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_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} }
 @misc{mondet_beaurepaire_mcafee_locke_alaux_blanchard_danka_le conte_2020, title={Honey bee survival mechanisms against the parasite Varroa destructor: a systematic review of phenotypic and genomic research efforts}, volume={50}, ISSN={["1879-0135"]}, DOI={10.1016/j.ijpara.2020.03.005}, abstractNote={The ectoparasitic mite Varroa destructor is the most significant pathological threat to the western honey bee, Apis mellifera, leading to the death of most colonies if left untreated. An alternative approach to chemical treatments is to selectively enhance heritable honey bee traits of resistance or tolerance to the mite through breeding programs, or select for naturally surviving untreated colonies. We conducted a literature review of all studies documenting traits of A. mellifera populations either selectively bred or naturally selected for resistance and tolerance to mite parasitism. This allowed us to conduct an analysis of the diversity, distribution and importance of the traits in different honey bee populations that can survive V. destructor globally. In a second analysis, we investigated the genetic bases of these different phenotypes by comparing ’omics studies (genomics, transcriptomics, and proteomics) of A. mellifera resistance and tolerance to the parasite. Altogether, this review provides a detailed overview of the current state of the research projects and breeding efforts against the most devastating parasite of A. mellifera. By highlighting the most promising traits of Varroa-surviving bees and our current knowledge on their genetic bases, this work will help direct future research efforts and selection programs to control this pest. Additionally, by comparing the diverse populations of honey bees that exhibit those traits, this review highlights the consequences of anthropogenic and natural selection in the interactions between hosts and parasites.}, number={6-7}, journal={INTERNATIONAL JOURNAL FOR PARASITOLOGY}, author={Mondet, Fanny and Beaurepaire, Alexis and McAfee, Alison and Locke, Barbara and Alaux, Cedric and Blanchard, Solene and Danka, Bob and Le Conte, Yves}, year={2020}, month={Jun}, pages={433–447} }
 @misc{traynor_mondet_miranda_techer_kowallik_oddie_chantawannakul_mcafee_2020, title={Varroa destructor: A Complex Parasite, Crippling Honey Bees Worldwide}, volume={36}, ISSN={["1471-5007"]}, DOI={10.1016/j.pt.2020.04.004}, abstractNote={The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honey bee (Apis cerana), to the naïve European honey bee (Apis mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honey bee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology, and management of varroa, and integrate older knowledge that is less well known.}, number={7}, journal={TRENDS IN PARASITOLOGY}, author={Traynor, Kirsten S. and Mondet, Fanny and Miranda, Joachim R. and Techer, Maeva and Kowallik, Vienna and Oddie, Melissa A. Y. and Chantawannakul, Panuwan and McAfee, Alison}, year={2020}, month={Jul}, pages={592–606} }
 @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{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} }