Molecular responses to stressors
Multiple, synergistically interacting factors underlie pollinator declines, including parasite and pathogen pressures, exposure to pesticides, reduced and poor quality nutrition due to the lack of abundance and diversity of flowering plant species, and climate change. We have examined the molecular, physiological and transcriptional responses of honey bees (Apis mellifera) to these many of these stressors, identifying conserved and unique transcriptional pathways responding to these different stressors. Interestingly, we have found that pathways involved in metabolic and nutritional processes are consistently regulated by different stressors. Moreover, we have found that providing pollen-based nutrition to bees can increase their resilience to different stressors. Additionally, we have found that transcriptional profiles can reliably reflect exposure to different stressors, and thus a “landscape transcriptomics” approach can be used to evaluate the stressors experienced by wild populations.
Selected References
Mokkapati, J.S. and C.M. Grozinger. Dietary lipids shape honey bee (Apis mellifera) feeding and resilience to pesticide stress. Journal of Insect Physiology, p.105021. https://doi.org/10.1016/j.jinsphys.2026.105021 (2026).
Ray, A.M., Tehel, A., Rasgon, J.L., Paxton, R.J., and C.M. Grozinger. “The intensity of the transcriptional response varies across infection with distinct viral strains in an insect host” BMC Genomics 26:175 https://doi.org/10.1186/s12864-025-11365-8 (2025).
Quinlan, G.M., Hines, H. M., and C.M. Grozinger, “Leveraging transcriptional signatures of diverse stressors for bumble bee conservation” Molecular Ecology 34(3):e17626. https://doi.org/10.1111/mec.17626 (2025)
Ray, A.M., Gordon, E.C., Seeley, T.D., Rasgon, J.L. and C.M. Grozinger. “Signatures of adaptive decreased virulence of deformed wing virus in an isolated population of wild honey bees (Apis mellifera)” Proceedings of the Royal Society B 290(2009). https://doi.org/10.1098/rspb.2023.1965 (2023)
Keagy, J, Drummond, C.P., Gilbert, K.J., Grozinger, C.M., Hamilton, J., Hines, H. M., Lasky, J., Logan, C.A., Sawers, R., and T. Wagner. “Landscape transcriptomics as a tool for addressing global change effects across diverse species” Molecular Ecology Resources https://doi.org/10.1111/1755-0998.13796 (2023)
Ray, A. M., Davis, S. L., Rasgon, J.L. and C.M. Grozinger. “Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera)” Journal of General Virology 102(11):001687 https://doi.org/10.1099/jgv.0.001687 (2021).
Crone, M.K. and C.M. Grozinger. “Pollen protein and lipid content influence resilience to insecticides in honey bees (Apis mellifera)”. Journal of Experimental Biology 224 (9): jeb242040 https://doi.org/10.1242/jeb.242040 (2021).
Ray, A.M., Lopez, D.L., Martinez, J.F., Galbraith, D.A., Rose, R., vanEngelsdorp, D., Rosa, C., Evans, J.D., and C.M. Grozinger. “Distribution of recently identified bee-infecting viruses in managed honey bee (Apis mellifera) populations in the United States” Apidologie DOI: 10.1007/s13592-020-00757-2 (2020).
Annoscia, D., Brown, S.P., Di Prisco, G., De Paoli, E., Del Fabbro, S.D., Frizzera, D., Zanni., V., Galbraith, D.A., Caprio, E., Grozinger, C.M., Pennachio, F. and F. Nazzi., "Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra’s model" Proc Roy Soc Bio 286 (1901), 20190331 (2019).
Grozinger C.M. and Flenniken, M.L. “Bee Viruses: Ecology, Pathogenicity, and Impacts”. Annual Review of Entomology 64: 205-226 (2019).
Kocher, O. Losyev, E. Muli, H. M. Patch, J. M. Sakamoto, S. Stanley, A. D. Vaudo and C. M. Grozinger. "Investigating the viral ecology of global bee communities with high-throughput metagenomics " Scientific Reports 8 (1): 8879 (2018).
Annoscia, D., Zanni., V., Galbraith, D., Quirici, A., Grozinger, C., Bortolomeazzi, R., Nazzi, F. “Elucidating the mechanisms underlying the beneficial health effects of dietary pollen on honey bees (Apis mellifera) infested by Varroa mite ectoparasites.” Scientific Reports 7: 6258(2017).
Zanni., V., Galbraith, D., Annoscia, D., Grozinger, C.M., Nazzi, F. “Transcriptional signatures of parasitization and markers of colony decline in Varroa-infested honey bees (Apis mellifera).” Insect Biochemistry and Molecular Biology 87: 1-13. (2017)
Doublet, V.*, Poeschl, Y.*, Gogol-Döring, A., Alaux, C., Annoscia, D., Aurori, C., Barribeau, S.M., Bedoya-Reina, O., Brown, M.J.F., Bull, J.C., Flenniken, M.L., Galbraith, D.A., Genersch, E., Gisder, S., Grosse, I., Holt, H.L., Hultmark, D., Lattorff, H.M.G., Le Conte, Y., Manfredini, F., McMahon, D.P., Moritz, R.F.A., Nazzi, F., Niño, E.L., Nowak, K., van Rij, R.P., Paxton, R.J.*, and C. M. Grozinger*. "Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens" BMC Genomics 18(1): 207 (2017). *indicates co-first authors and co-senior authors.
Schmehl, D. R., Teal, P.E.A., Frazier, J.F. and C. M. Grozinger. "Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera)". Journal of Insect Physiology 71: 177-190 (2014).
Holt, H.L., Aronstein, K. and C.M. Grozinger. “Chronic parasitization by the microsporidian Nosema causes global expression changes in core nutritional, metabolic, and behavioral pathways in honey bee workers (Apis mellifera)” BMC Genomics 14: 799 (2013).