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First published online August 23, 2004
Journal of Experimental Biology 207, 3281-3288 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01151

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Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor

Yehuda Ben-Shahar^1,*, Nichole L. Dudek^1, and Gene E. Robinson^1,2

¹ Department of Entomology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA
² Neuroscience Program, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA

View larger version (29K): [in a new window]   Fig. 1. Alignment of the D. melanogaster malvolio sequence with the putative A. mellifera ortholog (partial sequence). The two protein sequences are more than 80% similar for the sequence shown.

View larger version (21K): [in a new window]   Fig. 2. Behavioral development affects Amvl brain expression and manganese levels. (A) qRT-PCR analysis of Amvl expression in individual brains of nurses and foragers from triple-cohort colonies (in which bees display age-appropriate behavior; nurses were 7 days old; foragers were >21 days old). (B) qRT-PCR analysis of Amvl expression in individual brains of nurses and foragers from single-cohort colonies (in which some bees display precocious behavior; nurses and foragers 7-9 days old). (C) Manganese levels in individual heads of nurses and foragers from a triple-cohort colony (ages as in A). (D) Manganese levels in individual heads of nurses and precocious foragers from a single-cohort colony (ages as in B). Graphs represent means ± S.E.M. (converted to the same arbitrary scale as the mean) from ANOVA-adjusted pooled data of four independent colonies. Different letters above bars represent groups that were significantly different by the ANOVA Bonferroni post hoc analysis (P<0.05). Numbers in bars represent sample size.

View larger version (150K): [in a new window]   Fig. 3. Amvl expression in the honey bee brain. Antennal lobes (AL); Kenyon cells (KC); subesophageal ganglion (SOG). (A) Anterior coronal section, which includes the antennal lobes. Squares delineate regions shown magnified. (B) Posterior coronal section, which includes the SOG. No labeling was seen in control sections probed with a sense riboprobe (C). There were no obvious spatial differences in expression patterns between nurses and either forager type (N=3 brains per group); these images are from a pollen forager brain. Brains were sectioned from the anterior (AL) to the posterior end (SOG).

View larger version (17K): [in a new window]   Fig. 4. Manganese treatment affects sucrose responsiveness. (A) Effects of MnCl2, ZnCl2 and 8-Br-cGMP treatments on sugar responsiveness using the proboscis extension assay (Ben-Shahar and Robinson, 2001). 8-Br-cGMP was used to explore the relationship between sucrose responsiveness and rate of behavioral maturation (Ben-Shahar et al., 2002b). Bees were exposed to a sequential series of increasing sucrose concentration (see Materials and methods); a higher response index indicates increased responsiveness to sucrose. (B) Effect of manganese treatment on head manganese levels. Manganese levels increased significantly in heads of treated bees relative to untreated controls (P<0.001, ANOVA), validating the treatment method. Bars represent means ± S.E.M. Numbers in bars represent sample sizes. Results of statistical analysis in text. Different letters above bars represent groups that were significantly different by ANOVA with Bonferroni post hoc analysis (P<0.05). Numbers in bars represent pooled data from six independent trials (A).

View larger version (21K): [in a new window]   Fig. 5. Manganese treatment induces precocious foraging. (A) Effects of MnCl2, ZnCl2 and 8-Br-cGMP on age at onset of foraging. % initiating foraging refers to the percentage of bees from each treatment group that were observed to initiate foraging (data pooled from six individual experimental colonies; pooled numbers shown in key). (B) Effects of MnCl2, ZnCl2 and 8-Br-cGMP on tendency to collect pollen. Bars represent means ± S.E.M. of the percent of foragers from each colony returning with pollen. There was a significant difference among the treatment groups (P<0.05; PROC GENMOD; counts of foragers converted to percentages solely for graphical purposes), but no consistent trends were evident when examining the data for each colony (N=6; line graphs). Differences in the proportion of bees starting to forage from each treatment group were evaluated with multiple factor survival analysis with Cox proportional hazards estimation (Ben-Shahar et al., 2002b).