Christina Grozinger, Ph.D.
Distinguished Professor of Entomology
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Penn State Center and Program Affiliations
Intercollege Graduate Degree Program in Ecology
Intercollege Graduate Degree Program in Molecular, Cellular, and Integrative Biosciences
Center for Pollinator Research
Center for Chemical Ecology
Center for Brain, Behavior and Cognition
Center for Infectious Disease Dynamics
Current Graduate Students:
Holly Holt (NSF Graduate Fellow)
Alex McMenamin (Barry Goldwater Scholarship)
Aine O'Sullivan (University Graduate Fellow)
Anthony Vaudo (co-advised by John Tooker, USDA-NIFA Predoctoral Scholar)
Gabriel Villar (Sloan Scholar, USDA-NIFA Predoctoral Scholar)
Etya Amsalem (BARD Postdoctoral Fellow)
Research Interests :
Social insects, behavioral genomics, neuroethology, chemical ecology, disease ecology
ENT 597B Concepts and Techniques in Molecular Ecology (Spring 2013, with Harland Patch; awarded Penn State Harbaugh Faculty Scholars Program Award for Excellence in Teaching & Learning, offered in alternate years)
ENT 445 Evolution and Insect Societies (Spring 2012, with Mark Mescher, offered in alternate years)
ENT 530 Diversity in Science Seminar (Fall 2013, with Mary Barbercheck)
ENT 296A Honey Bees and Humans (Fall 2013, with Harland Patch and Maryann Frazier, offered annually).
ENT 522 Critical Thinking and Professional Development (Spring 2014, with Harland Patch, Jason Rasgon, and Jim Frazier, offered annually)
Research Activities & Interests:
My program seamlessly integrates research, education, outreach and service related to the biology and health of honey bees and other pollinators. My research addresses both basic and applied questions, using a highly trans-disciplinary approach encompassing genomics, physiology, neurobiology, behavior, and chemical ecology. My program consists of two main areas of study, which examine the mechanisms underlying social behavior and health in honey bees and related species. Our studies on social behavior seek to elucidate the proximate and ultimate mechanisms that regulate complex chemical communication systems in insect societies. Our studies on honey bee health examine how biotic and abiotic stressors impact the individual at the molecular, physiological and behavioral level, and have begun to examine how responses to these stressors can be modulated by social and environmental contexts.
Social behavior. Classically, studies of chemical communication in animals and plants have focused on identifying active chemical compounds and characterizing the behavioral responses to these signals. The initial investigations in my group sought to extend this work to the genomic level, and fully characterize the molecular mechanisms underlying responses of worker bees to the pheromone produced by queen bees. We demonstrated that exposure to queen pheromone caused changes in expression of genes and physiological pathways that were associated with the observed behavioral changes, even prior to or in the absence of expression of these behaviors. However, we also found that responses to queen pheromone were highly flexible. Such variability in pheromone responses and production had been noted previously in honey bees and other model systems, but the underlying mechanisms, and whether or not this variability was biologically relevant and under selection, had not been considered.
Through a series of published and ongoing studies, we demonstrated that responses of worker bees to queen pheromone are modulated by (1) physiological factors associated with behavioral maturation and (2) epigenetic, developmental and physiological factors associated with reproductive potential. Thus, as workers mature and transition between different tasks, their responses to the same pheromone change, and same-aged workers with higher reproductive potential are less responsive and less likely to perform “cooperative” behaviors. We are currently exploring a long-standing evolutionary question on whether intragenomic conflict between maternal and paternal alleles contributes to variation in worker reproductive potential. Furthermore, our comparative studies with bumble bees, wasps, and ants have found that social context strongly influences expression patterns – often more so than an individual’s physiological state – but the underlying sets of genes are not conserved across species.
We have also examined flexibility in the production of queen pheromone in honey bees. A key question in the evolution of communication systems is whether pheromones are ‘honest signals’ of an individual’s physiological state or dishonest, manipulative signals. Our studies suggested that different components of queen pheromone convey information about caste (worker vs queen), reproductive state (virgin, mated, laying), and mating quality (insemination substance and volume). Differences in pheromone profiles associated with mating quality are associated with altered behavioral and physiological responses in workers, which may impact overall colony structure and health. Ongoing studies aim to (1) identify the genes involved in pheromone biosynthetic pathways, (2) use genomic tools to identify seminal proteins which trigger these changes, (3) determine how rapidly the queen can alter pheromone production (4) examine how and why female and male responses to the same pheromone differ so profoundly.
Health. Studies of the impacts of stressors (pathogens, parasites, pesticides, nutrition) on honey bees have been relatively limited, primarily examining effects on longevity, simple behaviors or expression of a handful of immune response genes. We have substantially expanded our understanding of the impacts of these stressors by adopting a genomic approach. We have characterized genome-wide expression changes to “general” immunostimulants (beads, bacteria), and demonstrated that acute immune responses include a much broader array of genes than previous considered, including genes involved in key developmental pathways and pheromone production. Immunostimulation also alters bees’ chemical profiles, resulting in altered social interactions which may modulate disease spread. We currently examining the effects of natural parasites (Nosema), pathogens (viruses) and pesticides, and have found these significantly alter expression of core immune, physiological and behavioral pathways, including those involved in division of labor, suggesting that stressors impact overall colony organization. We will ultimately perform a meta-analysis to determine if bees employ common or distinct mechanisms to respond to different stressors. These results and our ongoing NSF-Gates Foundation funded BREAD project in Kenya suggest that metabolic pathways responsive to nutrition/diet are key components of common stress responses, and landscape ecology and foraging resources may buffer the effects of these stressors; future studies will address these hypotheses in more detail.
Relevant Publications: (Selected from 63 total)
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 (in press).
LeBoeuf, A. and C. M. Grozinger. " Me and we: the interplay between individual and group behavioral variation in social collectives." Current Opinion in Insect Science (in press).
Amsalem, E., Teal, P., Grozinger, C.M., and A. Hefetz. "Precocene-I inhibits juvenile hormone biosynthesis, ovarian activation, aggression and alters sterility signal production in bumble bee (Bombus terrestris) workers" Journal of Experimental Biology 217(17): 3178-3185 (2014).
Vaudo, A.D., Patch, H.M., Mortensen, D.A., Grozinger, C. M., and J. F. Tooker. "Bumble bees exhibit daily behavioral patterns in pollen foraging". Arthropod-Plant Interactions 8(4): 273-283 (2014).
Muli*, E., Patch*, H.M., Frazier*, M., Frazier, J., Torto, B., Baumgarten, T., Kilonzo, J., Kilmani, J., Mumoki, F., Masiga, D., Tumlinson, J., and C.M. Grozinger. "Evaluation of distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa" PLoS ONE 9(4): e94459 (2014).
Amsalem, E., Malka, O., Grozinger, C.M., and A. Hefetz. "Exploring the role of juvenile hormone and vitellogenin in reproduction and social behavior in bumble bees" BMC Evolutionary Biology 14:45 (2014).
Malka, O., Niño, E.L., Grozinger, C.M., and A. Hefetz. “Genomic analysis of the interactions between social environment and social communication systems in honey bees (Apis mellifera)” Insect Biochemistry and Molecular Biology 47: 36-45 (2014).
Toth, A.L., Tooker, J.F., Radhakrishnan, S., Minard, R., Henshaw, M.T., and C.M. Grozinger. “Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus)” BMC Genomics 15(1): 75 (2014).
Manfredini, F., Lucas, C., Nicolas, M., Keller, L., Shoemaker, D., and C.M. Grozinger. "Molecular and social regulation of worker division of labor in fire ants". Molecular Ecology 23(3): 660-672 (2014).
Cabrera, A.R., Shirk, P.D., Grozinger. C.M., Evans, J.D., and P. A. Teal. "Examining the role of foraging and malvolio in host-finding behavior in the honey bee parasite, Varroa destructor (Anderson & Trueman)". Archives of Insect Physiology and Biochemistry 85(2): 61-75 (2014).
Grozinger, C.M., Richards, J., and H. Mattila. "From molecules to societies: the mechanisms regulating swarming behavior in honey bees (Apis spp)" Apidologie 45:237-346 (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).
Niño, E.L., Malka, O., Hefetz, A. Tarpy, D.R., and C.M. Grozinger. Chemical profiles of two pheromone glands are differentially regulated by distinct mating factors in honey bee queens (Apis mellifera L.)" PLoS ONE 8(11): e78637 (2013).
Manfredini, F., Riba-Grognuz, O., Wurm, Y., Keller, L., Shoemaker, D.D., and C.M. Grozinger. "Sociogenomics of cooperation and conflict during colony founding in the fire ant, Solenopsis invicta" PLoS Genetics 9(8): e1003633 (2013).
Carbera, A.R., Shirk, P.D., Duehl, A.J., Donohue, K.V., Grozinger, C.M., Evans, J.D., and P.E.A. Teal. “Genomic organization and reproductive regulation of a large lipid transfer protein in the varroa mite, Varroa destructor (Anderson & Trueman)” Insect Molecular Biology 22(5): 505-522 (2013).
Weiner, S.A., Galbraith, D.A., Adams, D.C., Valenzuela, N., Noll, F.B., Grozinger, C.M. and A. L. Toth. "A survey of DNA methylation across social insect species, life stages, and castes reveals abundant and caste-associated methylation in a primitively social wasp" Naturwissenschaften 100(8): 795-799 (2013).
Niño, E.L., Tarpy, D.R., and C.M. Grozinger. “Differential effects of insemination volume and substance on reproductive changes in honey bee queens (Apis mellifera L.)” Insect Molecular Biology 22(3): 233-244 (2013).
Manfredini, F., Beani, L., and C.M. Grozinger. “Examining the ‘Evolution of increased competitive ability’ hypothesis in response to parasites and pathogens in the invasive paper wasps Polistes dominulus” Naturwissenschaften 100(3):219-28 (2013).
Nunes, F.M.F., Silva, A., Barchuk, A.R., Bomtorin, A.D., Grozinger, C.M. and Z.L.P. Simoes. “Non-target effects of double-stranded RNA constructs used in honey bee RNAi assays” Insects 4(1): 90-103 (2013).
Peso, M., Niño, E.L., Grozinger, C.M. and A. B. Barron. “Effect of honey bee queen mating condition on worker ovary activation” Insectes Sociaux 60(2): 123-133 (2013).
Richard, F.J., Holt, H.L., and C.M. Grozinger. “Effects of immunostimulation on genome-wide gene expression, chemical communication and social behavior in honey bee workers (Apis mellifera)” BMC Genomics 3:558, 17p (2012).
Cardoza, Y.J., Harris, G.K. and C.M. Grozinger. “Effects of soil quality enhancement on pollinator-plant interactions” Psyche 2012: 581458, 8p (2012). doi:10.1155/2012/581458
Niño, E.L., Malka, O., Hefetz, A., Teal, P., Hayes, J. and C.M. Grozinger. “Long-term effects of honey bee queen (Hymenoptera: Apis mellifera) insemination volume on queen-worker interactions” Journal of Insect Physiology 58(8):1082-1089 (2012).
Wang, Y., Kocher, S.D., Linksvayer T.A., Grozinger, C.M., Page, R.E., and G.V. Amdam. “Regulation of behaviorally-associated gene pathways in worker honey bee ovaries” Journal of Experimental Biology 215(1): 124-134 (2012).
J. Craig Williams