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The gene vitellogenin has multiple coordinating effects on social organization.

Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV - PLoS Biol. (2007)

Bottom Line: We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity.These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways.Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California Davis, Davis, California, United States of America.

ABSTRACT
Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.

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Effect of vitellogenin Gene Activity on Size of Nectar Loads CollectedKnockdowns (vgRNAi) collected more nectar than injected controls (injGFP; ANOVA, F1,315 = 6.79, p < 0.010). The difference between injected controls and non-injected reference (noREF) bees was also significant (ANOVA, F1,313 = 6.00, p< 0.015). Bars are means with standard errors.
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pbio-0050062-g003: Effect of vitellogenin Gene Activity on Size of Nectar Loads CollectedKnockdowns (vgRNAi) collected more nectar than injected controls (injGFP; ANOVA, F1,315 = 6.79, p < 0.010). The difference between injected controls and non-injected reference (noREF) bees was also significant (ANOVA, F1,313 = 6.00, p< 0.015). Bars are means with standard errors.

Mentions: In addition, down-regulation of vitellogenin gene activity (n = 160) resulted in foragers collecting larger loads of nectar relative to GFP dsRNA controls (n = 159, p < 0.010; see Figure 3 for details). Overall, loads were within the range normally collected by honeybees (up to 60-mg nectar and 30-mg pollen [16,17]), and thus interfering with vitellogenin expression did not change the maximum load size collected by workers. The observed bias towards nectar collection in vitellogenin knockdowns is consistent with earlier studies showing low hemolymph (blood) levels of vitellogenin in young worker bees from genetic stocks that preferentially collect nectar [9]. Genetic stocks with bias for collecting pollen are characterized by high levels of vitellogenin prior to foraging onset [9]. Our data, however, go beyond these correlations and demonstrate that the vitellogenin gene influences social foraging specialization.


The gene vitellogenin has multiple coordinating effects on social organization.

Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV - PLoS Biol. (2007)

Effect of vitellogenin Gene Activity on Size of Nectar Loads CollectedKnockdowns (vgRNAi) collected more nectar than injected controls (injGFP; ANOVA, F1,315 = 6.79, p < 0.010). The difference between injected controls and non-injected reference (noREF) bees was also significant (ANOVA, F1,313 = 6.00, p< 0.015). Bars are means with standard errors.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808115&req=5

pbio-0050062-g003: Effect of vitellogenin Gene Activity on Size of Nectar Loads CollectedKnockdowns (vgRNAi) collected more nectar than injected controls (injGFP; ANOVA, F1,315 = 6.79, p < 0.010). The difference between injected controls and non-injected reference (noREF) bees was also significant (ANOVA, F1,313 = 6.00, p< 0.015). Bars are means with standard errors.
Mentions: In addition, down-regulation of vitellogenin gene activity (n = 160) resulted in foragers collecting larger loads of nectar relative to GFP dsRNA controls (n = 159, p < 0.010; see Figure 3 for details). Overall, loads were within the range normally collected by honeybees (up to 60-mg nectar and 30-mg pollen [16,17]), and thus interfering with vitellogenin expression did not change the maximum load size collected by workers. The observed bias towards nectar collection in vitellogenin knockdowns is consistent with earlier studies showing low hemolymph (blood) levels of vitellogenin in young worker bees from genetic stocks that preferentially collect nectar [9]. Genetic stocks with bias for collecting pollen are characterized by high levels of vitellogenin prior to foraging onset [9]. Our data, however, go beyond these correlations and demonstrate that the vitellogenin gene influences social foraging specialization.

Bottom Line: We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity.These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways.Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California Davis, Davis, California, United States of America.

ABSTRACT
Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.

Show MeSH