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.  We have examined transcriptional, physiological and behavioral responses of honey bees (Apis mellifera) to bacteria [1, 2], Nosema microsporidia [3], Varroa mites [4, 5], viral infections [6], and pesticide exposure [7].  Together with an international consortium of researchers, we have recently synthesized data sets from 19 different transcriptomic studies to identify common and unique transcriptional responses to Nosema, viruses, and Varroa mites [8].  Our results have led to several novel findings, including that both parasite and pesticide stressors lead to changes in transcriptional pathways associated with metabolism and nutrition, and increasing nutritional quality can improve resilience to these stressors.  We also found that viral infection results in transcriptional and epigenetic (DNA methylation) changes in distinct suites of genes, suggesting that a previously uncharacterized epigenetic mechanism mediates responses to viruses.  Finally, our studies have led to the identification of a wealth of candidate genes – many which are not represented in the canonical insect immune response pathway -  which function in either conserved or unique responses to these stressors, and can be explored further for their biological function or can be targeted by breeding or RNAi approaches (eg, [9]) to help improve bee resilience and health.  In current studies, we are examining the responses of bees to newly identified viruses (see “Metagenomics studies of viral diversity”) and identified the molecular responses to and modes of action of pesticides to diverse bee species.

Current lab members: Allyson Ray, Makaylee Crone

Former lab members: Holly Holt, Elina Lastro Niño, Freddie-Jeanne Richard, Clare Rittschof, David Galbraith

Collaborators (Penn State): Dan Schmehl, Jim Tumlinson, David Biddinger, Rose Zhu

Collaborators: Judy Chen, Jay Evans, Francesco Nazzi, Robert Paxton (and the Trans-Bee consortium), Gene Robinson, Tom Webster, Soojin Yi,

Funding: USDA-NIFA-AFRI, USDA-NIFA-CAP, NSF-MCB, NSF Graduate Research Fellowship (Crone), Synthesis Centre for Biodiversity Sciences (sDiv)


 1. Richard FJ, Holt HL, Grozinger CM: Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 2012, 13:558.

2. Richard FJ, Aubert A, Grozinger CM: Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 2008, 6:50.

3. Holt HL, Aronstein KA, Grozinger CM: Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera). BMC Genomics 2013, 14:799.

4. 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 2017, 7: 6258.

5. 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 2017 87: 1-13.

6. Galbraith DA, Yang X, Nino EL, Yi S, Grozinger C: Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Pathog 2015, 11(3):e1004713.

7. Schmehl DR, Teal PE, Frazier JL, Grozinger CM: Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). J Insect Physiol 2014, 71:177-190.

8. Doublet V, Poeschl Y, Consortium atT: Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens. BMC Genomics submitted.

9. 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 2017 18(1): 207. *indicates co-first authors and co-senior authors.