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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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The Effect of vitellogenin RNAi on Hemolymph Vitellogenin ConcentrationsLevels are in micrograms per microliter relative to a β-galactosidase standard. Significant suppression of vitellogenin is apparent in RNAi knockdowns (vgRNAi) compared to injected controls (injGFP; Mann-Whitney U test: Z = 2.84, n = 54, p < 0.005). Control injections (GFP-derived dsRNA) did not significantly affect the vitellogenin level of the bees compared to the non-injected reference group (noREF; Mann-Whitney U test: Z = −1.10, n = 55, p = 0.27). Bars show results as means and standard errors with corresponding medians at the bottom of each bar. Because the dataset did not conform to assumptions of parametric tests (see Materials and Methods), medians can be considered the more accurate statistic. The dataset is split by age (10, 15 and 20 d olds) to visualize the persistence of RNAi. However, age did not affect the vitellogenin level of the workers (p = 0.68, see data analysis section for details), and thus conclusions cannot be drawn about treatment effects by age. The means and standard errors of the dataset overall are shown in the embedded box of the upper panel (medians for the dataset: noREF = 3.94, injGFP = 3.45, and vgRNAi = 2.46).
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pbio-0050062-g001: The Effect of vitellogenin RNAi on Hemolymph Vitellogenin ConcentrationsLevels are in micrograms per microliter relative to a β-galactosidase standard. Significant suppression of vitellogenin is apparent in RNAi knockdowns (vgRNAi) compared to injected controls (injGFP; Mann-Whitney U test: Z = 2.84, n = 54, p < 0.005). Control injections (GFP-derived dsRNA) did not significantly affect the vitellogenin level of the bees compared to the non-injected reference group (noREF; Mann-Whitney U test: Z = −1.10, n = 55, p = 0.27). Bars show results as means and standard errors with corresponding medians at the bottom of each bar. Because the dataset did not conform to assumptions of parametric tests (see Materials and Methods), medians can be considered the more accurate statistic. The dataset is split by age (10, 15 and 20 d olds) to visualize the persistence of RNAi. However, age did not affect the vitellogenin level of the workers (p = 0.68, see data analysis section for details), and thus conclusions cannot be drawn about treatment effects by age. The means and standard errors of the dataset overall are shown in the embedded box of the upper panel (medians for the dataset: noREF = 3.94, injGFP = 3.45, and vgRNAi = 2.46).

Mentions: The vitellogenin RNAi tool [12] was used in combination with observations of the behavior and lifespan of worker honeybees living in otherwise unmanipulated colonies. RNAi-mediated knockdown of the vitellogenin protein has been confirmed repeatedly in 5–7-d-old worker bees [3,5,12]. In this first RNAi study of honeybee social life history, however, we aimed to monitor workers over several weeks. Therefore, RNAi was validated in cohorts of 10-d-old (n = 31), 15-d-old (n = 27) and 20-d-old (n = 27) bees (Figure 1).


The gene vitellogenin has multiple coordinating effects on social organization.

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

The Effect of vitellogenin RNAi on Hemolymph Vitellogenin ConcentrationsLevels are in micrograms per microliter relative to a β-galactosidase standard. Significant suppression of vitellogenin is apparent in RNAi knockdowns (vgRNAi) compared to injected controls (injGFP; Mann-Whitney U test: Z = 2.84, n = 54, p < 0.005). Control injections (GFP-derived dsRNA) did not significantly affect the vitellogenin level of the bees compared to the non-injected reference group (noREF; Mann-Whitney U test: Z = −1.10, n = 55, p = 0.27). Bars show results as means and standard errors with corresponding medians at the bottom of each bar. Because the dataset did not conform to assumptions of parametric tests (see Materials and Methods), medians can be considered the more accurate statistic. The dataset is split by age (10, 15 and 20 d olds) to visualize the persistence of RNAi. However, age did not affect the vitellogenin level of the workers (p = 0.68, see data analysis section for details), and thus conclusions cannot be drawn about treatment effects by age. The means and standard errors of the dataset overall are shown in the embedded box of the upper panel (medians for the dataset: noREF = 3.94, injGFP = 3.45, and vgRNAi = 2.46).
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0050062-g001: The Effect of vitellogenin RNAi on Hemolymph Vitellogenin ConcentrationsLevels are in micrograms per microliter relative to a β-galactosidase standard. Significant suppression of vitellogenin is apparent in RNAi knockdowns (vgRNAi) compared to injected controls (injGFP; Mann-Whitney U test: Z = 2.84, n = 54, p < 0.005). Control injections (GFP-derived dsRNA) did not significantly affect the vitellogenin level of the bees compared to the non-injected reference group (noREF; Mann-Whitney U test: Z = −1.10, n = 55, p = 0.27). Bars show results as means and standard errors with corresponding medians at the bottom of each bar. Because the dataset did not conform to assumptions of parametric tests (see Materials and Methods), medians can be considered the more accurate statistic. The dataset is split by age (10, 15 and 20 d olds) to visualize the persistence of RNAi. However, age did not affect the vitellogenin level of the workers (p = 0.68, see data analysis section for details), and thus conclusions cannot be drawn about treatment effects by age. The means and standard errors of the dataset overall are shown in the embedded box of the upper panel (medians for the dataset: noREF = 3.94, injGFP = 3.45, and vgRNAi = 2.46).
Mentions: The vitellogenin RNAi tool [12] was used in combination with observations of the behavior and lifespan of worker honeybees living in otherwise unmanipulated colonies. RNAi-mediated knockdown of the vitellogenin protein has been confirmed repeatedly in 5–7-d-old worker bees [3,5,12]. In this first RNAi study of honeybee social life history, however, we aimed to monitor workers over several weeks. Therefore, RNAi was validated in cohorts of 10-d-old (n = 31), 15-d-old (n = 27) and 20-d-old (n = 27) bees (Figure 1).

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
Related in: MedlinePlus