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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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Vitellogenin Has a Dual Role in Regulation of Social BehaviorAfter the maturation phase, when bees are unable to forage (grey) [37], vitellogenin suppresses the transition from nest tasks to foraging activity when its titer remains above the foraging threshold level [3,7]. Below this threshold, the probability of initiating foraging is increased [5]. Pre-foraging vitellogenin titers above the pollen threshold prime workers for pollen foraging (green), while workers with lower pre-foraging titers (yellow) are primed for nectar foraging [9]. vitellogenin RNAi causes workers to mature with vitellogenin titers that are below both thresholds [3,7,9,12], resulting in the vitellogenin knockdown phenotype documented here: bees that forage precociously and preferentially collect nectar.
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pbio-0050062-g005: Vitellogenin Has a Dual Role in Regulation of Social BehaviorAfter the maturation phase, when bees are unable to forage (grey) [37], vitellogenin suppresses the transition from nest tasks to foraging activity when its titer remains above the foraging threshold level [3,7]. Below this threshold, the probability of initiating foraging is increased [5]. Pre-foraging vitellogenin titers above the pollen threshold prime workers for pollen foraging (green), while workers with lower pre-foraging titers (yellow) are primed for nectar foraging [9]. vitellogenin RNAi causes workers to mature with vitellogenin titers that are below both thresholds [3,7,9,12], resulting in the vitellogenin knockdown phenotype documented here: bees that forage precociously and preferentially collect nectar.

Mentions: Our results suggest that honeybee vitellogenin has an integrative function in regulating social organization through its pleiotropic effects on division of labor and foraging specialization. Vitellogenin inhibits the onset of foraging (our study) but declines with age in workers [8,20], thereby serving as a pacemaker for age polyethism and lifespan, as first hypothesized by Omholt and Amdam [7,21]. Higher titers early in life [9] prime bees for pollen collection, whereas low titers prime bees for collecting nectar (our study). vitellogenin RNAi established at adult emergence triggers persistent suppression of vitellogenin activity [3,5,12] (Figure 1), and therefore, the knockdown phenotype was expected to initiate foraging early, collect nectar, and live a short life (Figure 5).


The gene vitellogenin has multiple coordinating effects on social organization.

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

Vitellogenin Has a Dual Role in Regulation of Social BehaviorAfter the maturation phase, when bees are unable to forage (grey) [37], vitellogenin suppresses the transition from nest tasks to foraging activity when its titer remains above the foraging threshold level [3,7]. Below this threshold, the probability of initiating foraging is increased [5]. Pre-foraging vitellogenin titers above the pollen threshold prime workers for pollen foraging (green), while workers with lower pre-foraging titers (yellow) are primed for nectar foraging [9]. vitellogenin RNAi causes workers to mature with vitellogenin titers that are below both thresholds [3,7,9,12], resulting in the vitellogenin knockdown phenotype documented here: bees that forage precociously and preferentially collect nectar.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0050062-g005: Vitellogenin Has a Dual Role in Regulation of Social BehaviorAfter the maturation phase, when bees are unable to forage (grey) [37], vitellogenin suppresses the transition from nest tasks to foraging activity when its titer remains above the foraging threshold level [3,7]. Below this threshold, the probability of initiating foraging is increased [5]. Pre-foraging vitellogenin titers above the pollen threshold prime workers for pollen foraging (green), while workers with lower pre-foraging titers (yellow) are primed for nectar foraging [9]. vitellogenin RNAi causes workers to mature with vitellogenin titers that are below both thresholds [3,7,9,12], resulting in the vitellogenin knockdown phenotype documented here: bees that forage precociously and preferentially collect nectar.
Mentions: Our results suggest that honeybee vitellogenin has an integrative function in regulating social organization through its pleiotropic effects on division of labor and foraging specialization. Vitellogenin inhibits the onset of foraging (our study) but declines with age in workers [8,20], thereby serving as a pacemaker for age polyethism and lifespan, as first hypothesized by Omholt and Amdam [7,21]. Higher titers early in life [9] prime bees for pollen collection, whereas low titers prime bees for collecting nectar (our study). vitellogenin RNAi established at adult emergence triggers persistent suppression of vitellogenin activity [3,5,12] (Figure 1), and therefore, the knockdown phenotype was expected to initiate foraging early, collect nectar, and live a short life (Figure 5).

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