Christina Grozinger, Ph.D.

Current Graduate Students:

David Galbraith
Holly Holt
Elina Lastro Niño
Jessica Richards
Gabriel Villar
Anthony Vaudo

Postdoctoral Scholars:

Fabio Manfredini

Department Focus Area:

Genomics, Chemical Ecology

Research Interests :

Social insects, behavioral genomics, neuroethology, chemical ecology

Teaching:

• Genes and Behavior Seminar (Spring 2009, with Harland Patch)
• Evolution and Insect Societies (Spring 2010, with Mark Mescher)
• Concepts and Techniques in Molecular Ecology (Spring 2011, with Harland Patch; awarded Penn State Harbaugh Faculty Scholars Program Award for Excellence in Teaching & Learning

Research Activities & Interests:

Our research focuses on the genomic analysis of social behavior in honey bees and other social insect species. We are primarily interesting in understanding the molecular basis and evolution of chemical communication and host-parasite interactions. We are characterizing the molecular, physiological, behavioral, and social factors that regulate these processes.

These studies not only shed light on the molecular pathways underlying behavior, olfaction, immunity, and chemical ecology, but can also serve as the basis for applied research into novel methods for improving honey bee breeding, colony health and management.

This research seamlessly integrates behavioral studies (both in the field and in the lab), physiological assays, chemical ecology, functional genomics, and comparative studies. It provides an excellent platform for training students in interdisciplinary studies.

Honey bee queen biology.

Honey bee queens are the only reproductive individuals in a colony, and thus are critical for colony health and productivity. Queens also display a fascinating range of behavioral states, which we can access through behavioral observations or manipulations, such as instrumental insemination. Finally, queens produce a pheromone blend that plays a key role in organizing worker behavior and physiology.

We have demonstrated a close association between reproductive state and pheromone production. The overall chemical blend of the mandibular glands is modulated by reproductive state and insemination volume (Kocher et al 2008, Richard et al 2007), and correlates strongly with ovary activation (Kocher et al 2009). Furthermore, workers are more attracted to extracts of queens inseminated with semen from multiple drones or with higher levels of ovary activation.

We have also demonstrated that gene expression patterns in the brain, ovaries and fat bodies of queens are exquisitely sensitive to the overall reproductive physiology of the queen (Kocher et al 2008, Kocher et al 2010, Niño et al in press, Richard et al in prep). Furthermore, factors associated with instrumental insemination (volume, substance) can have long-terms effects on expression patterns, even after queens have initiated egg-laying.

Current studies are characterizing the genes and biosynthetic pathways involved in pheromone production (Malka, Grozinger and Hefetz, unpublished data), the effects of different stressors on queen behavior, physiology, and pheromone production (Schmehl, Grozinger and Tumlinson, unpublished data), and the volatile cues used by the queen during swarming events (Carr-Markell, Richards, Grozinger, Mattila, unpublished data).

These studies are in collaboration with David Tarpy (NCSU), Abraham Hefetz (University of Tel Aviv), James Tumlinson (Penn State), and Heather Mattila (Wellesley College), and have been supported by funding from the USDA-AFRI, NSF and the US-Israel Binational Science Foundation.

Genomics of pheromone response in social insects.

While responses to pheromones are typically considered to be instinctive and hard-wired, it is clear that responses can be modulated by environmental context, or the physiology and genotype of the receiving individual. We are examining the genes underlying modulation of responses to queen pheromone in honey bees, and the conservation of these pathways across other social insects, including bumble bees, paper wasps, and fire ants.

Queen mandibular pheromone (QMP) causes short and long-term behavioral and physiological changes in worker bees, and causes large scale changes in brain gene expression (Grozinger et al 2003). Short- and long-term responses QMP can be uncoupled; thus, they appear to operate by different mechanisms (Grozinger et al. 2007). Modulation of physiological state can also affect behavioral, physiological and genomic responses to QMP; factors associated with behavioral maturation, for example, can reduce responsiveness to QMP at all these levels (Grozinger and Robinson 2007, Fussnecker et al submitted). Interestingly, worker reproductive physiology is also correlated with behavioral responses, such that workers with greater reproductive potential are less attracted to the pheromone (Kocher et al 2010). We are using QTL analysis and microarrays to examine the genes regulating this individual variation in worker responses to QMP (Kocher et al 2010; Kocher et al in prep), and determining how this variation affects worker behavior in the colony and colony organization (Galbraith and Grozinger, unpublished data). Finally, some of the components of QMP also serve as a sex pheromone, regulating drone attraction to queens.  We are examining the molecular basis of this attraction (Villar and Grozinger, unpublished data).

We are also studying the evolution of queen-worker interactions. We are using molecular evolution studies to characterize this system in Apis (Kocher, Patch, et al in prep) and beginning to examine the conservation of QMP pheromone-response pathways in other social insects with similar colony organizations. Queen presence regulates expression of a QMP-responsive gene, Kr-h1, in both honey bees and bumble bees, and expression of this gene appears to be associated with modulation of JH-regulated pathways (Shpigler et al 2010). We are also using the fire ant genome to develop microarrays to identify the genes regulated by queen presence in this species, and determine how these response pathways are modulated by caste and genotype (Manfredini et al, unpublished data). Finally, we are examining the molecular bases of chemical communication and dominance hierarchies in paper wasps (Toth et al in prep).

These studies are in collaboration with Guy Bloch (Hebrew University of Jerusalem), Harland Patch (Penn State), Amy Toth (Iowa State), DeWayne Shoemaker (USDA), Laurent Keller (University of Lausanne, Switzerland), John Wang (BRACAS, Taiwan), Chip Aquadro (Cornell University), Greg Hunt (Purdue University), Miguel Arechavaleta-Velasco (INIFAP, Mexico), and have been supported by funding from the USDA-AFRI and NSF.

Social immunity.

 With the sequencing of the bee genome, it has become apparent that bees have fewer immune genes than solitary insects (Evans et al. 2006), suggesting that they use modified behavioral responses to control diseases and pests. Indeed, strains bred for resistance to Varroa mites have improved hygienic behavior, leading to reduced parasite load (ie, Harbo and Harris 2006). We have also demonstrated that nestmate recognition among workers bees is modulated by immunostimulation (Richard et al 2008). 

We are now characterizing the gene pathways involved in regulating responses to standard immune elicitors (Richard, Holt and Grozinger, in prep), parasites (Holt, Aronstein, Grozinger in prep), and viruses. We are examining the effects of caste and reproductive status on immune responses. Finally, we are surveying populations of honey bee subspecies in Kenya to determine if there is variation in parasite and pathogen load associated with genetic or geographic variation. 

These studies are in collaboration with Freddie-Jeanne Richard (University of Poitiers, France), Kate Aronstein (USDA), Eluid Muli and Dan Masiga (icipe, Kenya), Harland Patch, Maryann Frazier, James Frazier, and James Tumlison (Penn State), and have been supported by funding from the USDA-AFRI, USDA-CAPS and NSF-BREAD.

Relevant Publications:

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 (in press)

Richard, F.J., Schal, C. Tarpy, D.R., and C.M. Grozinger. “Effects of insemination number on honey bee queen Dufour’s gland secretion” Journal of Chemical Ecology 37(9):1027-36 (2011).

Fussnecker, B.L., McKenzie, A.M., and C.M. Grozinger. “The role of cGMP in modulating behavior, physiology, and brain gene expression in response to queen mandibular pheromone in honey bees” Journal of Comparative Physiology A 197(9): 939-948 (2011).  **publication with an undergraduate

Bloch, G. and C.M. Grozinger. “Social molecular pathways and the evolution of bee societies” Philosophical Transactions of the Royal Society B 366(1574): 2155-70 (2011).

Niño, E.L., Tarpy, D.R., and C.M. Grozinger. “Dissection of factors that trigger post-mating changes in honey bee queens (Apis mellifera L.)” Insect Molecular Biology. 20(3): 387-98 (2011).

Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JA, Andersson M, Andre JB, van Baalen M, Balloux F, Balshine S, Barton N, Beukeboom LW, Biernaskie JM, Bilde T, Borgia G, Breed M, Brown S, Bshary R, Buckling A, Burley NT, Burton-Chellew MN, Cant MA, Chapuisat M, Charnov EL, Clutton-Brock T, Cockburn A, Cole BJ, Colegrave N, Cosmides L, Couzin ID, Coyne JA, Creel S, Crespi B, Curry RL, Dall SR, Day T, Dickinson JL, Dugatkin LA, El Mouden C, Emlen ST, Evans J, Ferriere R, Field J, Foitzik S, Foster K, Foster WA, Fox CW, Gadau J, Gandon S, Gardner A, Gardner MG, Getty T, Goodisman MA, Grafen A, Grosberg R, Grozinger CM, Gouyon PH, Gwynne D, Harvey PH, Hatchwell BJ, Heinze J, Helantera H, Helms KR, Hill K, Jiricny N, Johnstone RA, Kacelnik A, Kiers ET, Kokko H, Komdeur J, Korb J, Kronauer D, Kümmerli R, Lehmann L, Linksvayer TA, Lion S, Lyon B, Marshall JA, McElreath R, Michalakis Y, Michod RE, Mock D, Monnin T, Montgomerie R, Moore AJ, Mueller UG, Noë R, Okasha S, Pamilo P, Parker GA, Pedersen JS, Pen I, Pfennig D, Queller DC, Rankin DJ, Reece SE, Reeve HK, Reuter M, Roberts G, Robson SK, Roze D, Rousset F, Rueppell O, Sachs JL, Santorelli L, Schmid-Hempel P, Schwarz MP, Scott-Phillips T, Shellmann-Sherman J, Sherman PW, Shuker DM, Smith J, Spagna JC, Strassmann B, Suarez AV, Sundström L, Taborsky M, Taylor P, Thompson G, Tooby J, Tsutsui ND, Tsuji K, Turillazzi S, Ubeda F, Vargo EL, Voelkl B, Wenseleers T, West SA, West-Eberhard MJ, Westneat DF, Wiernasz DC, Wild G, Wrangham R, Young AJ, Zeh DW, Zeh JA, Zink A. “Inclusive fitness theory and eusociality”. Nature 471(7339): E1-4 (2011).

Vasquez, G.M., Fischer, P., Grozinger, C.M. and F. Gould. “Differential expression of odorant receptor genes that are involved in sexual isolation of two Heliothis moths” Insect Molecular Biology 20(1): 115-124 (2011).

Grozinger, C.M. and Robinson, G.E. “Sociogenomics”. In: Breed, M.  and Moore, J. (eds.) Encyclopedia of Animal Behavior. Oxford: Elsevier Press. (2010)

Grozinger, CM.  “Genomic approaches to behavioral ecology and evolution”. In: Westneat DF and Fox, CW (eds.) Evolutionary Behavioral Ecology. New York City: Oxford University Press.  (2010).

Shpigler, H., Patch, H.M., Cohen, M., Fan, Y., Grozinger, C.M., and G. Bloch. “A gene for queen control: Krüppel homolog 1 is linked to social organization in bees” BMC Evolutionary Biology 10:120 (2010).

Kocher, S.D., Ayroles, J.F., Stone, E.A.  and C.M. Grozinger. “Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees” PLoS ONE 5(2): e9116 (2010).

Donohue, K.V, Khalil, S.M.S., Ross, E. Grozinger, C.M., Sonenshine, D.E. and R.M. Roe, "Neuropeptide signaling sequences identified by pyrosequencing of the American Dog tick synganglion transcriptome during blood-feeding and reproduction" Insect Biochemistry and Molecular Biology 40(1): 79-90 (2010).

Fan, Y., Richard, FJ., Rouf, C. and C.M. Grozinger. “Effects of queen mandibular pheromone on nestmate recognition in worker honey bees (Apis mellifera)” Animal Behavior 79(3): 649-656 (2010).

Kocher, S.D., Richard, F.J., Tarpy, D.R., and C.M. Grozinger.  "The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression" Insect Molecular Biology 19(2): 153-162 (2010).

Bloch, G. and Grozinger, C.M.  “Social molecular pathways, their origins, and modifications along the evolution of bee sociality. Philosophical Transactions of the Royal Society. (submitted)

Grozinger, C.M. and Robinson, G.E.  “Sociogenomics”. In: Breed, M.  and Moore, J. (eds.) Encyclopedia of Animal Behavior. Oxford: Elsevier Press. (in press)

Grozinger, CM.  Genomic approaches to behavioral ecology and evolution. In: Westneat DF and Fox, CW (eds.) Evolutionary Behavioral Ecology. New York City: Oxford University Press. (in press)

Kocher, S.D., Richard, F.J., Tarpy, D.R., and C.M. Grozinger.  “Queen reproductive state modulates queen pheromone production and queen-worker interactions in honey bees” Behavioral Ecology 20: 1007-1014 (2009)

Alaux, C., Y. Le Conte, H. Heather, S. Rodrigues-Zas, C.M. Grozinger, S. Sinha, and G. E. Robinson. “Regulation of brain gene expression in honey bees by brood pheromone” Genes, Brain, and Behavior 8(3):309-19 (2009).

Richard, F.J., A. Aubert, and C.M. Grozinger. “Modulation of nestmate recognition by immune stimulation in honey bees, Apis mellifera”. BMC Biology 6:50 (2008).

Fussnecker, B. and C.M. Grozinger. “Dissecting the role of Kr-h1 brain gene expression in foraging behavior in honey bees (Apis mellifera)”. Insect Molecular Biology. 17(5):515-22 (2008).

Kocher, S.D., Richard, F.J., Tarpy, D.R., and C.M. Grozinger. “Genomic analysis of post-mating changes in the honey bee queen”. BMC Genomics. 9(1):232 (2008).

Fischer, P. and C.M. Grozinger. “Pheromonal regulation of starvation resistance in honey bee workers”. Naturwissenschaften. 95(8):723-9 (2008).

Hornstein, E.D. “Longevity in the honeybee (Apis mellifera): expression of telomerase and insulin signaling pathway genes in queen and worker bees”. Journal of Young Investigators. Vol 18. (2008) (Mentor: C.M.G.; E. Hornstein was a high school student in my lab).

Richard, F.J., Tarpy, D.R, and C.M. Grozinger. “Effects of insemination quantity on honey bee queen physiology”. PLoS ONE , 2(10):e980 (2007).

Grozinger, C.M., Fan, Y., Hoover, S.E.R. and M.L. Winston. “Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera).” Molecular Ecology 16(22):4837-48 (2007).

Shi, L., Lin, S., Grinberg, Y., Beck, Y., Grozinger, C.M., Robinson, G.E. and T. Lee. “Roles of Drosophila Kruppel-homolog 1 in neuronal morphogenesis”. Dev Neurobiol. 67(12):1614-26 (2007).

Grozinger, C.M., Fischer, P, and J.E. Hampton. “Uncoupling primer and releaser responses to pheromone in honey bees.” Naturwissenschaften 94(5):375-9. (2007) **publication with undergraduates

Grozinger, C.M. and Robinson, G.E. “Endocrine modulation of a pheromone responsive gene in the honey bee brain” Journal of Comparative Biology A 193(4):461-70 (2007).

Honey Bee Genome Consortium (C.M.G., contributing author). “The genome of a highly social insect, the honey bee Apis mellifera.” Nature 443(7114):931-49 (2006).

Robinson, G.E., Grozinger, C.M., and Whitfield, C.W. (2005) “Social life in molecular terms.” Nat Gen Rev 6, 257-270.

Grozinger, C. M., Sharabash, N. M., Whitfield, C. W. and Robinson, G. E. (2003) “Pheromone mediated gene expression in the honey bee brain.” Proc Natl Acad Sci U S A 100 (Suppl 2),14519-25.