@article{nino_malka_hefetz_tarpy_grozinger_2013, title={Chemical Profiles of Two Pheromone Glands Are Differentially Regulated by Distinct Mating Factors in Honey Bee Queens (Apis mellifera L.)}, volume={8}, ISSN={["1932-6203"]}, DOI={10.1371/journal.pone.0078637}, abstractNote={Pheromones mediate social interactions among individuals in a wide variety of species, from yeast to mammals. In social insects such as honey bees, pheromone communication systems can be extraordinarily complex and serve to coordinate behaviors among many individuals. One of the primary mediators of social behavior and organization in honey bee colonies is queen pheromone, which is produced by multiple glands. The types and quantities of chemicals produced differ significantly between virgin and mated queens, and recent studies have suggested that, in newly mated queens, insemination volume or quantity can affect pheromone production. Here, we examine the long-term impact of different factors involved during queen insemination on the chemical composition of the mandibular and Dufour's glands, two of the major sources of queen pheromone. Our results demonstrate that carbon dioxide (an anesthetic used in instrumental insemination), physical manipulation of genital tract (presumably mimicking the act of copulation), insemination substance (saline vs. semen), and insemination volume (1 vs. 8 µl) all have long-term effects on mandibular gland chemical profiles. In contrast, Dufour's gland chemical profiles were changed only upon insemination and were not influenced by exposure to carbon dioxide, manipulation, insemination substance or volume. These results suggest that the chemical contents of these two glands are regulated by different neuro-physiological mechanisms. Furthermore, workers responded differently to the different mandibular gland extracts in a choice assay. Although these studies must be validated in naturally mated queens of varying mating quality, our results suggest that while the chemical composition of Dufour's gland is associated with mating status, that of the mandibular glands is associated with both mating status and insemination success. Thus, the queen appears to be signaling both status and reproductive quality to the workers, which may impact worker behavior and physiology as well as social organization and productivity of the colony.}, number={11}, journal={PLOS ONE}, author={Nino, Elina L. and Malka, Osnat and Hefetz, Abraham and Tarpy, David R. and Grozinger, Christina M.}, year={2013}, month={Nov} } @article{nino_tarpy_grozinger_2013, title={Differential effects of insemination volume and substance on reproductive changes in honey bee queens (Apis mellifera L.)}, volume={22}, ISSN={["1365-2583"]}, DOI={10.1111/imb.12016}, abstractNote={Abstract}, number={3}, journal={INSECT MOLECULAR BIOLOGY}, author={Nino, E. L. and Tarpy, D. R. and Grozinger, C. M.}, year={2013}, month={Jun}, pages={233–244} } @article{richard_holt_grozinger_2012, title={Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera)}, volume={13}, journal={BMC Genomics}, author={Richard, F. J. and Holt, H. L. and Grozinger, C. M.}, year={2012} } @article{vasquez_fischer_grozinger_gould_2011, title={Differential expression of odorant receptor genes involved in the sexual isolation of two Heliothis moths}, volume={20}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2010.01044.x}, abstractNote={Abstract}, number={1}, journal={INSECT MOLECULAR BIOLOGY}, author={Vasquez, G. M. and Fischer, P. and Grozinger, C. M. and Gould, F.}, year={2011}, month={Feb}, pages={115–124} } @article{richard_schal_tarpy_grozinger_2011, title={Effects of Instrumental Insemination and Insemination Quantity on Dufour’s Gland Chemical Profiles and Vitellogenin Expression in Honey Bee Queens (Apis mellifera)}, volume={37}, ISSN={0098-0331 1573-1561}, url={http://dx.doi.org/10.1007/s10886-011-9999-z}, DOI={10.1007/s10886-011-9999-z}, abstractNote={Honey bee queens (Apis mellifera) mate in their early adult lives with a variable number of males (drones). Mating stimulates dramatic changes in queen behavior, physiology, gene expression, and pheromone production. Here, we used virgin, single drone- (SDI), and multi-drone- (MDI) inseminated queens to study the effects of instrumental insemination and insemination quantity on the pheromone profiles of the Dufour's gland, and the expression of the egg-yolk protein, vitellogenin, in the fat body. Age, environmental conditions, and genetic background of the queens were standardized to specifically characterize the effects of these treatments. Our data demonstrate that insemination and insemination quantity significantly affect the chemical profiles of the Dufour's gland secretion. Moreover, workers were more attracted to Dufour's gland extract from inseminated queens compared to virgins, and to the extract of MDI queens compared to extract of SDI queens. However, while there were differences in the amounts of some esters between MDI queens and the other groups, it appears that the differences in behavioral responses were elicited by subtle changes in the overall chemical profiles rather than dramatic changes in specific individual chemicals. We also found a decrease in vitellogenin gene expression in the fat body of the MDI queens, which is negatively correlated with the quantities of Dufour's gland content. The possible explanations of this reduction are discussed.}, number={9}, journal={Journal of Chemical Ecology}, publisher={Springer Science and Business Media LLC}, author={Richard, Freddie-Jeanne and Schal, Coby and Tarpy, David R. and Grozinger, Christina M.}, year={2011}, month={Jul}, pages={1027–1036} } @article{nino_tarpy_grozinger_2011, title={Genome-wide analysis of brain transcriptional changes in honey bee (Apis mellifera L.) queens exposed to carbon dioxide and physical manipulation}, volume={20}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2011.2011.01072.x}, abstractNote={Mating is a complex process causing many behavioural and physiological changes, but the factors triggering them and the underlying molecular processes are not well characterized. In the present study we examine the effects of CO2 (a commonly used anaesthetic in instrumental insemination that causes changes similar to those occurring after mating) and physical manipulation (which may mimic certain aspects of copulation) on the behavioural, physiological and brain transcriptional changes in honey bee queens. We show that while CO2 causes cessation of mating flights and ovary activation, physical manipulation has additional effects on ovary activation and brain transcriptional changes. Comparisons with previous studies of honey bees and female Drosophila indicate that common molecular mechanisms may be responsible for regulating reproductive changes across different mating regimes and insect orders.}, number={3}, journal={INSECT MOLECULAR BIOLOGY}, author={Nino, E. L. and Tarpy, D. R. and Grozinger, C.}, year={2011}, month={Jun}, pages={387–398} } @article{fussnecker_mckenzie_grozinger_2011, title={cGMP modulates responses to queen mandibular pheromone in worker honey bees}, volume={197}, number={9}, journal={Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology}, author={Fussnecker, B. L. and McKenzie, A. M. and Grozinger, C. M.}, year={2011}, pages={939–948} } @article{fan_richard_rouf_grozinger_2010, title={Effects of queen mandibular pheromone on nestmate recognition in worker honeybees, Apis mellifera}, volume={79}, number={3}, journal={Animal Behaviour}, author={Fan, Y. L. and Richard, F. J. and Rouf, N. and Grozinger, C. M.}, year={2010}, pages={649–656} } @article{kocher_ayroles_stone_grozinger_2010, title={Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees}, volume={5}, number={2}, journal={PLoS One}, author={Kocher, S. D. and Ayroles, J. F. and Stone, E. A. and Grozinger, C. M.}, year={2010} } @article{donohue_khalil_ross_grozinger_sonenshine_roe_2010, title={Neuropeptide signaling sequences identified by pyrosequencing of the American dog tick synganglion transcriptome during blood feeding and reproduction}, volume={40}, ISSN={["1879-0240"]}, DOI={10.1016/j.ibmb.2009.12.014}, abstractNote={Ticks are important vectors of numerous pathogens that impact human and animal health. The tick central nervous system represents an understudied area in tick biology and no tick synganglion-specific transcriptome has been described to date. Here we characterize whole or partial cDNA sequences of fourteen putative neuropeptides (allatostatin, insulin-like peptide, ion-transport peptide, sulfakinin, bursicon alpha/beta, eclosion hormone, glycoprotein hormone alpha/beta, corazonin, four orcokinins) and five neuropeptide receptors (gonadotropin receptor, leucokinin-like receptor, sulfakinin receptor, calcitonin receptor, pyrokinin receptor) translated from cDNA synthesized from the synganglion of unfed, partially fed and replete female American dog ticks, Dermacentor variabilis. Their homology to the same neuropeptides in other taxa is discussed. Many of these neuropeptides such as an allatostatin, insulin-like peptide, eclosion hormone, bursicon alpha and beta and glycoprotein hormone alpha and beta have not been previously described in the Chelicerata. An insulin-receptor substrate protein was also found indicating that an insulin signaling network is present in ticks. A putative type-2 proprotein processing convertase was also sequenced that may be involved in cleavage at monobasic and dibasic endoproteolytic cleavage sites in prohormones. The possible physiological role of the proteins discovered in adult tick blood feeding and reproduction will be discussed.}, number={1}, journal={INSECT BIOCHEMISTRY AND MOLECULAR BIOLOGY}, author={Donohue, Kevin V. and Khalil, Sayed M. S. and Ross, E. and Grozinger, Christina M. and Sonenshine, Daniel E. and Roe, R. Michael}, year={2010}, month={Jan}, pages={79–90} } @article{kocher_tarpy_grozinger_2010, title={The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression}, volume={19}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2009.00965.x}, abstractNote={Abstract}, number={2}, journal={INSECT MOLECULAR BIOLOGY}, author={Kocher, S. D. and Tarpy, D. R. and Grozinger, C. M.}, year={2010}, month={Apr}, pages={153–162} } @article{shpigler_patch_cohen_fan_grozinger_bloch_2010, title={The transcription factor Kruppel homolog 1 is linked to hormone mediated social organization in bees}, volume={10}, journal={BMC Evolutionary Biology}, author={Shpigler, H. and Patch, H. M. and Cohen, M. and Fan, Y. L. and Grozinger, C. M. and Bloch, G.}, year={2010} } @article{kocher_richard_tarpy_grozinger_2009, title={Queen reproductive state modulates pheromone production and queen-worker interactions in honeybees}, volume={20}, ISSN={["1465-7279"]}, DOI={10.1093/beheco/arp090}, abstractNote={The mandibular glands of queen honeybees produce a pheromone that modulates many aspects of worker honeybee physiology and behavior and is critical for colony social organization. The exact chemical blend produced by the queen differs between virgin and mated, laying queens. Here, we investigate the role of mating and reproductive state on queen pheromone production and worker responses. Virgin queens, naturally mated queens, and queens instrumentally inseminated with either semen or saline were collected 2 days after mating or insemination. Naturally mated queens had the most activated ovaries and the most distinct chemical profile in their mandibular glands. Instrumentally inseminated queens were intermediate between virgins and naturally mated queens for both ovary activation and chemical profiles. There were no significant differences between semen- and saline-inseminated queens. Workers were preferentially attracted to the mandibular gland extracts from queens with significantly more activated ovaries. These studies suggest that the queen pheromone blend is modulated by the reproductive status of the queens, and workers can detect these subtle differences and are more responsive to queens with higher reproductive potential. Furthermore, it appears as if insemination substance does not strongly affect physiological characteristics of honeybee queens 2 days after insemination, suggesting that the insemination process or volume is responsible for stimulating these early postmating changes in honeybee queens.}, number={5}, journal={BEHAVIORAL ECOLOGY}, author={Kocher, Sarah D. and Richard, Freddie-Jeanne and Tarpy, David R. and Grozinger, Christina M.}, year={2009}, pages={1007–1014} } @article{alaux_le conte_adams_rodriguez-zas_grozinger_sinha_robinson_2009, title={Regulation of brain gene expression in honey bees by brood pheromone}, volume={8}, ISSN={["1601-183X"]}, DOI={10.1111/j.1601-183X.2009.00480.x}, abstractNote={ Pheromones are very important in animal communication. To learn more about the molecular basis of pheromone action, we studied the effects of a potent honey bee pheromone on brain gene expression. Brood pheromone (BP) caused changes in the expression of hundreds of genes in the bee brain in a manner consistent with its known effects on behavioral maturation. Brood pheromone exposure in young bees causes a delay in the transition from working in the hive to foraging, and we found that BP treatment tended to upregulate genes in the brain that are upregulated in bees specialized on brood care but downregulate genes that are upregulated in foragers. However, the effects of BP were age dependent; this pattern was reversed when older bees were tested, consistent with the stimulation of foraging by BP in older bees already competent to forage. These results support the idea that one way that pheromones influence behavior is by orchestrating large‐scale changes in brain gene expression. We also found evidence for a relationship between cis and BP regulation of brain gene expression, with several cis‐regulatory motifs statistically overrepresented in the promoter regions of genes regulated by BP. Transcription factors that target a few of these motifs have already been implicated in the regulation of bee behavior. Together these results demonstrate strong connections between pheromone effects, behavior, and regulation of brain gene expression. }, number={3}, journal={GENES BRAIN AND BEHAVIOR}, author={Alaux, C. and Le Conte, Y. and Adams, H. A. and Rodriguez-Zas, S. and Grozinger, C. M. and Sinha, S. and Robinson, G. E.}, year={2009}, month={Apr}, pages={309–319} } @article{fussnecker_grozinger_2008, title={Dissecting the role of Kr-h1 brain gene expression in foraging behavior in honey bees (Apis mellifera)}, volume={17}, ISSN={["1365-2583"]}, DOI={10.1111/j.1365-2583.2008.00819.x}, abstractNote={Abstract}, number={5}, journal={INSECT MOLECULAR BIOLOGY}, author={Fussnecker, B. and Grozinger, C.}, year={2008}, month={Oct}, pages={515–522} } @article{kocher_richard_tarpy_grozinger_2008, title={Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera)}, volume={9}, ISSN={["1471-2164"]}, DOI={10.1186/1471-2164-9-232}, abstractNote={Abstract}, journal={BMC GENOMICS}, author={Kocher, Sarah D. and Richard, Freddie-Jeanne and Tarpy, David R. and Grozinger, Christina M.}, year={2008}, month={May} } @article{richard_aubert_grozinger_2008, title={Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers}, volume={6}, journal={BMC Biology}, author={Richard, F. J. and Aubert, A. and Grozinger, C. M.}, year={2008} } @article{fischer_grozinger_2008, title={Pheromonal regulation of starvation resistance in honey bee workers (Apis mellifera)}, volume={95}, number={8}, journal={Naturwissenschaften (Berlin, Germany)}, author={Fischer, P. and Grozinger, C. M.}, year={2008}, pages={723–729} } @article{grozinger_robinson_2007, title={Endocrine modulation of a pheromone-responsive gene in the honey bee brain}, volume={193}, ISSN={["0340-7594"]}, DOI={10.1007/s00359-006-0202-x}, abstractNote={Pheromones cause dramatic changes in behavior and physiology, and are critical for honey bee colony organization. Queen mandibular pheromone (QMP) regulates multiple behaviors in worker bees (Slessor et al. in J Chem Ecol 31(11):2731-2745, 2005). We also identified genes whose brain expression levels were altered by exposure to QMP (Grozinger et al. in Proc Natl Acad Sci USA 100(Suppl 2):14519-14525, 2003). Krüppel-homolog 1 (Kr-h1) RNA levels were significantly downregulated by QMP, and were higher in foragers than in nurses (Whitfield et al. in Science 302(5643):296-299, 2003). Here we report on results of behavioral and pharmacological experiments that characterize factors regulating expression of Kr-h1. Foragers have higher brain levels of Kr-h1 than in-hive bees, regardless of age and pheromone exposure. Furthermore, forager Kr-h1 levels were not affected by QMP. Since the onset of foraging is caused, in part, by increasing juvenile hormone blood titers and brain octopamine levels, we investigated the effects of octopamine and methoprene (a juvenile hormone analog) on Kr-h1 expression. Methoprene produced a marginal (not significant) increase in Kr-h1 expression, but Kr-h1 brain levels in methoprene-treated bees were no longer downregulated by QMP. Octopamine did not modulate Kr-h1 expression. Our results demonstrate that the gene expression response to QMP is not hard-wired in the brain but is instead dependent on worker behavioral state.}, number={4}, journal={JOURNAL OF COMPARATIVE PHYSIOLOGY A-NEUROETHOLOGY SENSORY NEURAL AND BEHAVIORAL PHYSIOLOGY}, author={Grozinger, Christina M. and Robinson, Gene E.}, year={2007}, month={Apr}, pages={461–470} } @article{grozinger_fan_hoover_winston_2007, title={Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera)}, volume={16}, ISSN={["1365-294X"]}, DOI={10.1111/j.1365-294X.2007.03545.x}, abstractNote={Abstract}, number={22}, journal={MOLECULAR ECOLOGY}, author={Grozinger, Christina M. and Fan, Yongliang and Hoover, Shelley E. R. and Winston, Mark L.}, year={2007}, month={Nov}, pages={4837–4848} } @article{shi_lin_grinberg_beck_grozinger_robinson_lee_2007, title={Roles of Drosophila Kruppel-Homolog 1 in neuronal morphogenesis}, volume={67}, ISSN={["1932-846X"]}, DOI={10.1002/dneu.20537}, abstractNote={Abstract}, number={12}, journal={DEVELOPMENTAL NEUROBIOLOGY}, author={Shi, Lei and Lin, Suewei and Grinberg, Yelena and Beck, Yannick and Grozinger, Christina M. and Robinson, Gene E. and Lee, Tzumin}, year={2007}, month={Oct}, pages={1614–1626} } @article{grozinger_fischer_hampton_2007, title={Uncoupling primer and releaser responses to pheromone in honey bees}, volume={94}, number={5}, journal={Naturwissenschaften (Berlin, Germany)}, author={Grozinger, C. M. and Fischer, P. and Hampton, J. E.}, year={2007}, pages={375–379} } @misc{weinstock_robinson_gibbs_2006, title={Insights into social insects from the genome of the honeybee Apis mellifera}, volume={443}, number={7114}, journal={Nature}, author={Weinstock, G. M. and Robinson, G. E. and Gibbs, R. A.}, year={2006}, pages={931–949} }