The Effects of Fat Body Tyramine Level on Gustatory Responsiveness of Honeybees (Apis mellifera) Differ between Behavioral Castes

Division of labor is a hallmark of social insects. In the honeybee (Apis mellifera) each sterile female worker performs a series of social tasks. The most drastic changes in behavior occur when a nurse bee, who takes care of the brood and the queen in the hive, transitions to foraging behavior. Foragers provision the colony with pollen, nectar or water. Nurse bees and foragers differ in numerous behaviors, including responsiveness to gustatory stimuli. Differences in gustatory responsiveness, in turn, might be involved in regulating division of labor through differential sensory response thresholds. Biogenic amines are important modulators of behavior. Tyramine and octopamine have been shown to increase gustatory responsiveness in honeybees when injected into the thorax, thereby possibly triggering social organization. So far, most of the experiments investigating the role of amines on gustatory responsiveness have focused on the brain. The potential role of the fat body in regulating sensory responsiveness and division of labor has large been neglected. We here investigated the role of the fat body in modulating gustatory responsiveness through tyramine signaling in different social roles of honeybees. We quantified levels of tyramine, tyramine receptor gene expression and the effect of elevating fat body tyramine titers on gustatory responsiveness in both nurse bees and foragers. Our data suggest that elevating the tyramine titer in the fat body pharmacologically increases gustatory responsiveness in foragers, but not in nurse bees. This differential effect of tyramine on gustatory responsiveness correlates with a higher natural gustatory responsiveness of foragers, with a higher tyramine receptor (Amtar1) mRNA expression in fat bodies of foragers and with lower baseline tyramine titers in fat bodies of foragers compared to those of nurse bees. We suggest that differential tyramine signaling in the fat body has an important role in the plasticity of division of labor through changing gustatory responsiveness.

[1]  A. Barron,et al.  Learning, gustatory responsiveness and tyramine differences across nurse and forager honeybees , 2017, Journal of Experimental Biology.

[2]  A. Baumann,et al.  AmTAR2: Functional characterization of a honeybee tyramine receptor stimulating adenylyl cyclase activity. , 2017, Insect biochemistry and molecular biology.

[3]  R. Scheiner,et al.  Division of labour in honey bees: age‐ and task‐related changes in the expression of octopamine receptor genes , 2014, Insect molecular biology.

[4]  H. Scholz,et al.  Octopamine indirectly affects proboscis extension response habituation in Drosophila melanogaster by controlling sucrose responsiveness. , 2014, Journal of insect physiology.

[5]  R. Scheiner,et al.  PKG in honey bees: Spatial expression, Amfor gene expression, sucrose responsiveness, and division of labor , 2014, The Journal of comparative neurology.

[6]  A. Baumann,et al.  Molecular, pharmacological, and signaling properties of octopamine receptors from honeybee (Apis mellifera) brain , 2014, Journal of neurochemistry.

[7]  A. Barron,et al.  Differences in the phototaxis of pollen and nectar foraging honey bees are related to their octopamine brain titers , 2014, Front. Physiol..

[8]  A. Barron,et al.  Cocaine Tolerance in Honey Bees , 2013, PloS one.

[9]  R. Scheiner,et al.  Suitability of three common reference genes for quantitative real-time PCR in honey bees , 2012, Apidologie.

[10]  G. Amdam,et al.  Gustatory Perception and Fat Body Energy Metabolism Are Jointly Affected by Vitellogenin and Juvenile Hormone in Honey Bees , 2012, PLoS genetics.

[11]  R. Scheiner,et al.  Octopamine improves learning in newly emerged bees but not in old foragers , 2012, Journal of Experimental Biology.

[12]  G. Amdam,et al.  Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology , 2011, Journal of Experimental Biology.

[13]  G. Arnold,et al.  Effects of patriline on gustatory responsiveness and olfactory learning in honey bees , 2011, Apidologie.

[14]  Ying Wang,et al.  Nutritional regulation of division of labor in honey bees: toward a systems biology perspective , 2010, Wiley interdisciplinary reviews. Systems biology and medicine.

[15]  R. Scheiner,et al.  Behavioral Neuroscience , 2022 .

[16]  Brian R. Johnson,et al.  Division of labor in honeybees: form, function, and proximate mechanisms , 2009, Behavioral Ecology and Sociobiology.

[17]  G. Amdam,et al.  Impaired tactile learning is related to social role in honeybees , 2009, Journal of Experimental Biology.

[18]  G. Robinson,et al.  Regulation of brain gene expression in honey bees by brood pheromone , 2009, Genes, brain, and behavior.

[19]  G. Amdam,et al.  Cognitive aging is linked to social role in honey bees (Apis mellifera) , 2007, Experimental Gerontology.

[20]  Robert E. Page,et al.  Behavioral genomics of honeybee foraging and nest defense , 2006, Naturwissenschaften.

[21]  J. Erber,et al.  Phototactic behaviour correlates with gustatory responsiveness in honey bees (Apis mellifera L.) , 2006, Behavioural Brain Research.

[22]  A. Baumann,et al.  Aminergic control and modulation of honeybee behaviour. , 2006, Current neuropharmacology.

[23]  G. Amdam,et al.  Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera) , 2006, Behavioural Brain Research.

[24]  PROTEIN CONTENT AND AMINO ACID COMPOSITION OF BEE-COLLECTED POLLEN FROM SELECTED BOTANICAL ORIGINS , 2006 .

[25]  Gene E Robinson,et al.  Nutritional status influences socially regulated foraging ontogeny in honey bees , 2005, Journal of Experimental Biology.

[26]  Gene E. Robinson,et al.  Worker nutrition and division of labour in honeybees , 2005, Animal Behaviour.

[27]  T. Roeder.  Tyramine and octopamine: ruling behavior and metabolism. , 2005, Annual review of entomology.

[28]  R. Scheiner.  Responsiveness to sucrose and habituation of the proboscis extension response in honey bees , 2004, Journal of Comparative Physiology A.

[29]  R. E. Page,et al.  Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera) , 2004 .

[30]  P. Ebert,et al.  Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain , 2003, Journal of neurochemistry.

[31]  J. Erber,et al.  Variation in water and sucrose responsiveness during the foraging season affects proboscis extension learning in honey bees , 2003 .

[32]  Gene E. Robinson,et al.  A Role for Octopamine in Honey Bee Division of Labor , 2003, Brain, Behavior and Evolution.

[33]  Ricarda Scheiner,et al.  Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees , 2002, Behavioural Brain Research.

[34]  Robert E. Page,et al.  The Effects of Genotype, Foraging Role, and Sucrose Responsiveness on the Tactile Learning Performance of Honey Bees (Apis mellifera L.) , 2001, Neurobiology of Learning and Memory.

[35]  J. Erber,et al.  Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains , 2001, Behavioural Brain Research.

[36]  A. Baumann,et al.  Amtyr1: characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. , 2000, Journal of neurochemistry.

[37]  J. Erber,et al.  Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.) , 1999, Journal of Comparative Physiology A.

[38]  G. Robinson,et al.  Effects of colony food shortage on behavioral development in honey bees , 1998, Behavioral Ecology and Sociobiology.

[39]  T. Smith,et al.  Phenethylamine and related compounds in plants , 1977 .