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First published online June 29, 2006
Journal of Experimental Biology 209, 2774-2784 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02296

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Division of labor in the honey bee (Apis mellifera): the role of tyramine ß-hydroxylase

Herman K. Lehman^1,2,*, David J. Schulz⁴, Andrew B. Barron⁴, Lydia Wraight⁴, Chris Hardison^1,2, Sandra Whitney¹, Hideaki Takeuchi³, Rajib K. Paul³ and Gene E. Robinson^4,5

¹ Department of Biology, Hamilton College, Clinton, NY 13323, USA
² Program in Neuroscience, Hamilton College, Clinton, NY 13323, USA
³ Department of Biological Sciences, University of Tokyo, Tokyo, Japan
⁴ Department of Entomology,, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
⁵ Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

View larger version (20K): [in a new window]   Fig. 1. Octopamine (OA) levels in honey bee brains. OA levels for bees from single-cohort colonies (normal-aged nurses and precocious foragers) and typical colonies (typical foragers and typical nurses) are shown. Values are mean ± s.e.m.; sample size is indicated in each bar. *Significant differences between nurses and foragers (ANOVA and Fisher PLSD post-hoc tests). The results of two-way ANOVA for OA levels as a function of behaviour and colony type are also shown. Three trials were performed; the single-cohort colony was derived from the typical colony in each trial, and colonies in different trials were unrelated to each other.

View larger version (12K): [in a new window]   Fig. 2. Reverse-phase HPLC radiochromatograms of the enzymatic products from incubation of honey bee brain extracts with [ring-3H]tyramine. Large arrowhead indicates the elution of synthetic OA and the small arrow indicates the elution of synthetic tyramine as detected by electrochemical detection. Dark trace: radiochromatogram of the enzymatic products from untreated brain extracts. Light trace: compounds recovered from boiled enzyme reaction.

View larger version (26K): [in a new window]   Fig. 3. Tyramine ß-hydroxylase (T ßh) activity in honey bee brains. T ßh activity from bees from single-cohort colonies (SCC, normal-aged nurses and precocious foragers) and typical colonies (TC, typical foragers and typical nurses) are shown. Values are mean ± s.e.m.; sample size is indicated in each bar. *Significant differences between nurses and foragers (ANOVA and Fisher PLSD post-hoc tests). The results of two-way ANOVAs for T ßh activity as a function of behavior and colony type are also shown. Seven trials were performed; see Fig. 1 legend.

View larger version (85K): [in a new window]   Fig. 4. Nucleotide and deduced amino acid sequence of Apis T ßh. The first nucleotide and amino acid residue of the translational start site are designated as position 1. The amino acid positions of DOMON and Cu2+ type II ascorbate-dependent monoxygenase domains predicted by Scansite 2.0 (Obenauer et al., 2003) are indicated by italic bold and bold text, respectively. The nucleic acid sequences in white text on a black background are the regions used to synthesize the DIG-labeled antisense RNA probe for aTßh in situ hybridization procedures. The nucleic acid sequences used as primers for quantitative real-time PCR analysis are shown in black text on a grey background and the sequence used as a probe is shown in underlined black text on a grey background.

View larger version (19K): [in a new window]   Fig. 5. Tßh gene expression in honey bee brains. Cycle threshold (Ct) was determined using second derivative analysis and the difference in Ct between AmTßh and a control gene was used to determine relative expression levels. aTßh mRNA levels from single bees collected from single-cohort colonies (normal-aged nurses and precocious foragers) and typical colonies (typical foragers and typical nurses) are shown. Values are means ± s.e.m.; sample size is indicated in each bar. *Significant differences between nurses and foragers (ANOVA and Fisher PLSD post-hoc tests). Results of two-way ANOVA for T ßh expression as a function of behavior and colony type are also shown. Three trials were conducted (the same trials as in Fig. 1, and corresponding to Trials 1, 2 and 3 of Fig. 3).

View larger version (100K): [in a new window]   Fig. 6. Tßh gene localization in honey bee brains revealed by in situ hybridization. In situ hybridization was performed on nurses and foragers using 10 µm sections but only brains from nurses are shown here. Control experiments using DIG-labeled sense probes gave no significant signals in any of the in situ hybridization experiments (data not shown). (A) Frontal view of anterior (left), middle (middle) and posterior portion of the section (right). Areas corresponding to B-G are boxed. (B-G) Signals are indicated by arrows. m, medulla; lo, lobula; AL, antennal lobe; OES, esophagus; SOG, subesophageal ganglion. ICa, mushroom body lateral calyces; MCa, mushroom body medial calyces. Bars indicate 100 µm.