@article{mcafee_metz_connor_du_allen_frausto_swenson_phillips_julien_rempel_et al._2025, title={Factors affecting heat resilience of drone honey bees (<i>Apis mellifera</i>) and their sperm}, volume={20}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0317672}, number={2}, journal={PLOS ONE}, author={Mcafee, Alison and Metz, Bradley N. and Connor, Patrick and Du, Keana and Allen, Christopher W. and Frausto, Luis A. and Swenson, Mark P. and Phillips, Kylah S. and Julien, Madison and Rempel, Zoe and et al.}, year={2025}, month={Feb} }
 @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={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{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{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{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{metz_chakrabarti_sagili_2021, title={Honey Bee (Hymenoptera: Apidae) Nursing Responses to Cuticular Cues Emanating from Short-term Changes in Larval Rearing Environment}, volume={21}, ISSN={["1536-2442"]}, DOI={10.1093/jisesa/ieab085}, abstractNote={Honey bee larvae are dependent on the social structure of colony for their provisioning and survival. With thousands of larvae being managed collectively by groups of foragers (collecting food resources) and nurse bees (processing food and provisioning larvae), coordination of colony efforts in rearing brood depends on multiple dynamic cues of larval presence and needs. Much of these cues appear to be chemical, with larvae producing multiple pheromones, major being brood ester pheromone (BEP; nonvolatile blend of fatty acid esters) that elicits both short-term releaser effects and long-term primer effects. While BEP can affect colony food collection and processing with the signaling of larval presence, it is unclear if BEP signals individual larval needs. To understand this aspect, in a series of experiments we manipulated larval feeding environment by depriving larvae from adult bee contact for 4-h period and examined (1) nurse bee interactions with contact-deprived and nondeprived larvae and larval extracts; (2) forager bee responses to contact-deprived and nondeprived larval extracts. We also characterized BEP of contact-deprived and nondeprived larvae. We found that nurse honey bees tend to aggregate more over contact-deprived larvae when compared with nondeprived larvae, but that these effects were not found in response to whole hexane extracts. Our analytical results suggest that BEP components changed in both quantity and quality over short period of contact deprivation. These changes affected foraging behavior, but did not appear to directly affect nursing behavior, suggesting that different chemical cues are involved in regulating nursing effort to individual larvae.}, number={6}, journal={JOURNAL OF INSECT SCIENCE}, author={Metz, Bradley N. and Chakrabarti, Priyadarshini and Sagili, Ramesh R.}, year={2021}, month={Nov} }
 @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={Abstract 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{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={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{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{metz_wu-smart_simone-finstrom_2020, title={Proceedings of the 2020 American Bee Research Conference}, volume={11}, ISSN={["2075-4450"]}, DOI={10.3390/insects11060362}, abstractNote={The 2020 American Bee Research Conference (ABRC) was held on 9-10 January 2020 in conjunction with the annual convention of the American Beekeeping Federation Conference and Trade Show in Schaumburg, IL. Over the two-day conference, a total of 65 oral and poster presentations were given, representing work done from over 30 different research groups from throughout the United States and Canada. These proceedings contain the submitted abstracts for presentations given at the 2020 American Bee Research Conference.}, number={6}, journal={INSECTS}, author={Metz, Bradley N. and Wu-Smart, Judy and Simone-Finstrom, Michael}, year={2020}, month={Jun} }
 @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{sagili_metz_lucas_chakrabarti_breece_2018, title={Honey bees consider larval nutritional status rather than genetic relatedness when selecting larvae for emergency queen rearing}, volume={8}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-018-25976-7}, abstractNote={Abstract In honey bees and many other social insects, production of queens is a vital task, as colony fitness is dependent on queens. The factors considered by honey bee workers in selecting larvae to rear new queens during emergency queen rearing are poorly understood. Identifying these parameters is critical, both in an evolutionary and apicultural context. As female caste development in honey bees is dependent on larval diet (i.e. nutrition), we hypothesized that larval nutritional state is meticulously assessed and used by workers in selection of larvae for queen rearing. To test this hypothesis, we conducted a series of experiments manipulating the nutritional status of one day old larvae by depriving them of brood food for a four-hour period, and then allowing workers to choose larvae for rearing queens from nutritionally deprived and non-deprived larvae. We simultaneously investigated the role of genetic relatedness in selection of larvae for queen rearing. In all the experiments, significantly greater numbers of non-deprived larvae than deprived larvae were selected for queen rearing irrespective of genetic relatedness. Our results demonstrate that honey bees perceive the nutritional state of larvae and use that information when selecting larvae for rearing queens in the natural emergency queen replacement process.}, journal={SCIENTIFIC REPORTS}, author={Sagili, Ramesh R. and Metz, Bradley N. and Lucas, Hannah M. and Chakrabarti, Priyadarshini and Breece, Carolyn R.}, year={2018}, month={May} }