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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 LifespanCumulative hazard increases until all bees have died. Injected controls (injGFP) lived longer than knockdowns (vgRNAi; LRT = 4.38, df = 1, p < 0.036, hazard ratio [comparative survival experience calculated over the entire time of the study] = 1.29 d longer, confidence interval = 1.02–1.63 d). Longevity was affected by laboratory handling (LRT = 43.4, df = 1, p < 0.0001, hazard ratio = 1.96 d longer for non-injected reference (noREF) bees compared with injGFP bees, confidence interval = 1.61–2.38 d).
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pbio-0050062-g004: Effect of vitellogenin Gene Activity on LifespanCumulative hazard increases until all bees have died. Injected controls (injGFP) lived longer than knockdowns (vgRNAi; LRT = 4.38, df = 1, p < 0.036, hazard ratio [comparative survival experience calculated over the entire time of the study] = 1.29 d longer, confidence interval = 1.02–1.63 d). Longevity was affected by laboratory handling (LRT = 43.4, df = 1, p < 0.0001, hazard ratio = 1.96 d longer for non-injected reference (noREF) bees compared with injGFP bees, confidence interval = 1.61–2.38 d).

Mentions: Survival data showed that vitellogenin also is involved in the regulation of honeybee lifespan. Lifespan was reduced in vitellogenin knockdowns (n = 122) compared with GFP dsRNA controls (n = 179, p < 0.036, see Figure 4 for details). The effect was not due simply to bees initiating foraging behavior earlier in life, because these traits were not correlated in the knockdown phenotype (r = 0.121 [Colony 1]; r = −0.003 [Colony 2], p > 0.05). Our finding is supported by the previous results showing that worker bees with reduced vitellogenin activity levels are more susceptible to oxidative stress [4], a physiological state that is an established indicator of aging [18,19].


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 LifespanCumulative hazard increases until all bees have died. Injected controls (injGFP) lived longer than knockdowns (vgRNAi; LRT = 4.38, df = 1, p < 0.036, hazard ratio [comparative survival experience calculated over the entire time of the study] = 1.29 d longer, confidence interval = 1.02–1.63 d). Longevity was affected by laboratory handling (LRT = 43.4, df = 1, p < 0.0001, hazard ratio = 1.96 d longer for non-injected reference (noREF) bees compared with injGFP bees, confidence interval = 1.61–2.38 d).
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0050062-g004: Effect of vitellogenin Gene Activity on LifespanCumulative hazard increases until all bees have died. Injected controls (injGFP) lived longer than knockdowns (vgRNAi; LRT = 4.38, df = 1, p < 0.036, hazard ratio [comparative survival experience calculated over the entire time of the study] = 1.29 d longer, confidence interval = 1.02–1.63 d). Longevity was affected by laboratory handling (LRT = 43.4, df = 1, p < 0.0001, hazard ratio = 1.96 d longer for non-injected reference (noREF) bees compared with injGFP bees, confidence interval = 1.61–2.38 d).
Mentions: Survival data showed that vitellogenin also is involved in the regulation of honeybee lifespan. Lifespan was reduced in vitellogenin knockdowns (n = 122) compared with GFP dsRNA controls (n = 179, p < 0.036, see Figure 4 for details). The effect was not due simply to bees initiating foraging behavior earlier in life, because these traits were not correlated in the knockdown phenotype (r = 0.121 [Colony 1]; r = −0.003 [Colony 2], p > 0.05). Our finding is supported by the previous results showing that worker bees with reduced vitellogenin activity levels are more susceptible to oxidative stress [4], a physiological state that is an established indicator of aging [18,19].

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