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Effects of Flight on Gene Expression and Aging in the Honey Bee Brain and Flight Muscle.

Margotta JW, Mancinelli GE, Benito AA, Ammons A, Roberts SP, Elekonich MM - Insects (2012)

Bottom Line: To investigate the effects of flight, behavioral state and age on gene expression, we used whole-genome microarrays and real-time PCR.Our data suggest that the transition from behaviors requiring little to no flight (nursing) to those requiring prolonged flight bouts (foraging), rather than the amount of previous flight per se, has a major effect on gene expression.Combined with our real-time PCR data, these data suggest an epigenetic control and energy balance role in honey bee functional senescence.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Nevada, Las Vegas, NV 89154, USA. margotta@unlv.nevada.edu.

ABSTRACT
Honey bees move through a series of in-hive tasks (e.g., "nursing") to outside tasks (e.g., "foraging") that are coincident with physiological changes and higher levels of metabolic activity. Social context can cause worker bees to speed up or slow down this process, and foragers may revert back to their earlier in-hive tasks accompanied by reversion to earlier physiological states. To investigate the effects of flight, behavioral state and age on gene expression, we used whole-genome microarrays and real-time PCR. Brain tissue and flight muscle exhibited different patterns of expression during behavioral transitions, with expression patterns in the brain reflecting both age and behavior, and expression patterns in flight muscle being primarily determined by age. Our data suggest that the transition from behaviors requiring little to no flight (nursing) to those requiring prolonged flight bouts (foraging), rather than the amount of previous flight per se, has a major effect on gene expression. Following behavioral reversion there was a partial reversion in gene expression but some aspects of forager expression patterns, such as those for genes involved in immune function, remained. Combined with our real-time PCR data, these data suggest an epigenetic control and energy balance role in honey bee functional senescence.

No MeSH data available.


Unique and shared transcripts. Venn diagrams were used to visualize transcripts unique and shared between each group. Numbers represent transcripts differentially expressed (FDR < 0.05). (A) Transcripts differentially expressed between young bees, old bees and reverted nurse bees. (B) Transcripts differentially expressed between nurse bees. (C) Transcripts differentially expressed between forager bees. YN = young nurse (8–10 days-old; <1 day flight); RN = reverted nurse (25–26 days-old; 7–9 days flight); OF = old forager (25–26 days-old; 10–12 days flight); TH = typical-aged forager-high flight (19–22 days old; 7–9 days flight); ON = older nurse (19–22 days old; <1 day flight); TL = typical-aged forager-low flight (19–22 days old; 2–3 days flight); PF = precocious forager (8–10 days old; 2–3 days flight).
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insects-04-00009-f003: Unique and shared transcripts. Venn diagrams were used to visualize transcripts unique and shared between each group. Numbers represent transcripts differentially expressed (FDR < 0.05). (A) Transcripts differentially expressed between young bees, old bees and reverted nurse bees. (B) Transcripts differentially expressed between nurse bees. (C) Transcripts differentially expressed between forager bees. YN = young nurse (8–10 days-old; <1 day flight); RN = reverted nurse (25–26 days-old; 7–9 days flight); OF = old forager (25–26 days-old; 10–12 days flight); TH = typical-aged forager-high flight (19–22 days old; 7–9 days flight); ON = older nurse (19–22 days old; <1 day flight); TL = typical-aged forager-low flight (19–22 days old; 2–3 days flight); PF = precocious forager (8–10 days old; 2–3 days flight).

Mentions: We used a two-way ANOVA to find transcriptional differences between young bees, older bees and reverted nurse bees as well as between different aged nurses and between different aged foragers. Statistically significant differences in transcript expression were found by using the false discovery rate for multiple comparisons. Figure 3A shows which differentially expressed transcripts were unique to each age comparison and which transcripts overlapped. We found 684 differentially expressed transcripts unique to young bees (PF and YN) compared to old bees (OF and ON) and 231 transcripts unique to young bees (PF and YN) compared to reverted nurse bees (RN). This result implies only a small subset of the genes differentially transcribed during the nurse-to-forager transition do not revert during reversion from forager to nurse. There were no unique transcripts when old (OF and ON) bees were compared to reverted nurse bees (RN). When we analyzed what transcripts were unique within nurses and within foragers (Figure 3B,C), we found that foragers had more differentially expressed transcripts than aged-matched nurses, indicating that gene expression varies with age and behavior but flight has a greater effect on gene expression than age. This result is not surprising because flight produces high levels of reactive oxygen species and flight muscle antioxidant capacity decreases with age [18], both of which may lead to changes in gene expression.


Effects of Flight on Gene Expression and Aging in the Honey Bee Brain and Flight Muscle.

Margotta JW, Mancinelli GE, Benito AA, Ammons A, Roberts SP, Elekonich MM - Insects (2012)

Unique and shared transcripts. Venn diagrams were used to visualize transcripts unique and shared between each group. Numbers represent transcripts differentially expressed (FDR < 0.05). (A) Transcripts differentially expressed between young bees, old bees and reverted nurse bees. (B) Transcripts differentially expressed between nurse bees. (C) Transcripts differentially expressed between forager bees. YN = young nurse (8–10 days-old; <1 day flight); RN = reverted nurse (25–26 days-old; 7–9 days flight); OF = old forager (25–26 days-old; 10–12 days flight); TH = typical-aged forager-high flight (19–22 days old; 7–9 days flight); ON = older nurse (19–22 days old; <1 day flight); TL = typical-aged forager-low flight (19–22 days old; 2–3 days flight); PF = precocious forager (8–10 days old; 2–3 days flight).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4553427&req=5

insects-04-00009-f003: Unique and shared transcripts. Venn diagrams were used to visualize transcripts unique and shared between each group. Numbers represent transcripts differentially expressed (FDR < 0.05). (A) Transcripts differentially expressed between young bees, old bees and reverted nurse bees. (B) Transcripts differentially expressed between nurse bees. (C) Transcripts differentially expressed between forager bees. YN = young nurse (8–10 days-old; <1 day flight); RN = reverted nurse (25–26 days-old; 7–9 days flight); OF = old forager (25–26 days-old; 10–12 days flight); TH = typical-aged forager-high flight (19–22 days old; 7–9 days flight); ON = older nurse (19–22 days old; <1 day flight); TL = typical-aged forager-low flight (19–22 days old; 2–3 days flight); PF = precocious forager (8–10 days old; 2–3 days flight).
Mentions: We used a two-way ANOVA to find transcriptional differences between young bees, older bees and reverted nurse bees as well as between different aged nurses and between different aged foragers. Statistically significant differences in transcript expression were found by using the false discovery rate for multiple comparisons. Figure 3A shows which differentially expressed transcripts were unique to each age comparison and which transcripts overlapped. We found 684 differentially expressed transcripts unique to young bees (PF and YN) compared to old bees (OF and ON) and 231 transcripts unique to young bees (PF and YN) compared to reverted nurse bees (RN). This result implies only a small subset of the genes differentially transcribed during the nurse-to-forager transition do not revert during reversion from forager to nurse. There were no unique transcripts when old (OF and ON) bees were compared to reverted nurse bees (RN). When we analyzed what transcripts were unique within nurses and within foragers (Figure 3B,C), we found that foragers had more differentially expressed transcripts than aged-matched nurses, indicating that gene expression varies with age and behavior but flight has a greater effect on gene expression than age. This result is not surprising because flight produces high levels of reactive oxygen species and flight muscle antioxidant capacity decreases with age [18], both of which may lead to changes in gene expression.

Bottom Line: To investigate the effects of flight, behavioral state and age on gene expression, we used whole-genome microarrays and real-time PCR.Our data suggest that the transition from behaviors requiring little to no flight (nursing) to those requiring prolonged flight bouts (foraging), rather than the amount of previous flight per se, has a major effect on gene expression.Combined with our real-time PCR data, these data suggest an epigenetic control and energy balance role in honey bee functional senescence.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Nevada, Las Vegas, NV 89154, USA. margotta@unlv.nevada.edu.

ABSTRACT
Honey bees move through a series of in-hive tasks (e.g., "nursing") to outside tasks (e.g., "foraging") that are coincident with physiological changes and higher levels of metabolic activity. Social context can cause worker bees to speed up or slow down this process, and foragers may revert back to their earlier in-hive tasks accompanied by reversion to earlier physiological states. To investigate the effects of flight, behavioral state and age on gene expression, we used whole-genome microarrays and real-time PCR. Brain tissue and flight muscle exhibited different patterns of expression during behavioral transitions, with expression patterns in the brain reflecting both age and behavior, and expression patterns in flight muscle being primarily determined by age. Our data suggest that the transition from behaviors requiring little to no flight (nursing) to those requiring prolonged flight bouts (foraging), rather than the amount of previous flight per se, has a major effect on gene expression. Following behavioral reversion there was a partial reversion in gene expression but some aspects of forager expression patterns, such as those for genes involved in immune function, remained. Combined with our real-time PCR data, these data suggest an epigenetic control and energy balance role in honey bee functional senescence.

No MeSH data available.